Ultrastructure of the eye in fetal type II glycogenosis (Pompe's disease)
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1 Ultrastructure of the eye in fetal type II glycogenosis (Pompe's disease) Kathryn Stein Pokorny, Robert Ritch, Alan H. Friedman, and Robert J. Desnick* Type II glycogenosis is an autosomal recessive storage disease characterized by absence of the enzyme acid a-l,4-glucosidase. The eye of a 16 week fetus, aborted after diagnosis by amniocentesis, tvas studied by light and electron microscopy. Extensive deposits oflysosomal and. cytoplasmic glycogen were present in virtually all ocular tissues examined, with the notable exception of pigment epithelia (iris and retina). The massive glycogen deposits present in this, the youngest case thus far examined histologically, emphasize the involvement of the fetus from its earliest stages and the importance of prenatal diagnosis. (INVEST OPHTHALMOL VIS SCI 22: 25-31, 1982.) Key words: Pompe's disease, glycogenosis, lysosomal storage disease, silver proteinate, glycogen deposition, acid a-l,4-glucosidase, ocular involvement, fetus I ompe's disease (type II glycogenosis) is an autosomal recessive, lysosomal storage disease resulting from the deficient activity of the enzyme acid a-l,4-glucosidase (acid maltase). 1 The enzymatic defect leads to an accumulation of cellular glycogen, primarily lysosomal. 2 " 4 Although heart and skeletal From the Department of Ophthalmology and *Division of Medical Genetics, Mount Sinai School of Medicine of the City University of New York. This investigation was supported in part by National Institutes of Health grant RR71 of the Clinical Research Centers Program of the Division of Research Resources and grants EY and GM-25279, by an unrestricted grant from Research to Prevent Blindness, Inc., N.Y., by the National Society to Prevent Blindness, Inc., N.Y., and by grant from the National Foundation March of Dimes. Dr. Ritch is the recipient of an N.I.H. Academic Investigator Award EY Dr. Desnick is the recipient of an N.I.H. Research Career Development Award L-K04-AM Submitted for publication Jan. 18, Reprint requests: Kathryn S. Pokorny, Ph.D., Department of Ophthalmology, Mount Sinai School of Medicine, One Gustave Levy PI.; New York, N.Y muscle usually show the most marked pathologic and clinical involvement, glycogen deposition is also evident in virtually every tissue of the body, including brain, liver, pancreas, kidney, skin, and eye. 4 " 7 ' 18 Three major clinical subtypes of Pompe's disease have been identified 8 : (1) an infantile form, characterized by severe muscle involvement and cardiomegaly, leading to death from cardiorespiratory failure during the first few months of life; (2) a late infantile (or juvenile) form, similar in nature but more slowly progressive the patients usually dying during childhood; and (3) an adult form, presenting primarily with muscle weakness and characterized by a partial deficiency of acid a-l,4-glucosidase activity. 9 " 11 Fetuses with any form of the disease may be diagnosed prenatally. 12 " 14 Ultrastructural findings of each form of Pompe's have been reported. 2-3> }, Ocular findings in Pompe's disease are those of widespread glycogen deposits. 16> 18 " 20 Previous examination by light microscopy on infantile Pompe's showed a generalized accumulation of glycogen in the eye. 18 Ultra /82/ $00.70/ Assoc. for Res. in Vis. and Ophthal, Inc. 25
2 26 Pokorny et at. Invest. Ophthalmol, Vis. Sci. January 1982 INi Bm Fig. 1. Micrograph showing basal epithelium of conjunctiva with membrane-delimited accumulations of glycogen {large arrows) and free, cytoplasmic glycogen (small arrows). Architecture of cells appears normal except for these deposits. N, Nucleus; Bm, basement membrane. (Uranyl-lead stain; X9239.) structural analyses have been done for retina from the infantile form, on extraocular muscle from a late-infantile form, 21 and on ocular tissue from a 22-week-old fetus. 16 All studies indicated glycogen deposits at the fine structural level. We report the ultrastructural findings from the eye of a fetus that was selectively aborted after a 16 week gestation, thus providing information on the early pattern of ocular involvement in this inborn error of metabolism. Case report The fetus was the result of a second pregnancy of a woman whose first child died at 2 years of age from enzymatically documented type II glycogenosis. The parents received genetic counseling concerning the risk of this disease in a subsequent child. Prenatal diagnosis of Pompe's disease was made by the demonstration of deficient acid glucosidase activity in cultured amniotic cells. The parents re- Fig. 2. Micrograph showing conjunctival epithelium with intermediate stages in development of glycogen-engorged lysosomes (arrows). Note membrane surrounded accumulations of both glycogen and homogeneously electron-dense material. G, Glycogen. (Uranyl-lead stain; x27,300.) quested termination of the pregnancy, which was done at 16 weeks gestation by dilation and extraction. Materials and methods Fixation of the eyes for light and electron microscopy was accomplished by use of a trialdehyde fixative 22-2:i containing 1% each of glutaraldehyde, acrolein, and paraformaldehyde in 0.1M sodium cacodylate buffer with 5 mm CaCl 2, ph 7.4, for a minimum of 1 hr in the cold. Light microscopy. After fixation, tissue was processed routinely, embedded in paraffin, and cut at 8 /u.m. Sections were then stained with periodic acid- Schiff (PAS), Masson's trichrome, or hematoxylin-eosin (H & E). Diastase sensitivity was tested on sections later stained with PAS, with controls. Electron microscopy. After initial fixation, tissue was rinsed in 0.1M cacodylate buffer containing 0.5% NaCl; it was then postfixed for 1 hr in the cold in 1% osmium tetroxide in 0.1M cacodylate buffer, ph 7.4, dehydrated through a graded ethanol series to propylene oxide, and embedded in Epon. Thick (1 /xm) plastic sections were stained for metachromasia and orientation with
3 Volume 22 Number 1 Ultrastructure of eye in Pompe's disease 27 IM Fig. 3. Micrograph showing glycogen-filled lysosomes in conjunctival fibroblast. Glycogen particles can be seen bridging the gap through an opening in the membrane. Arrows show cytoplasmic particles of glycogen. (Silver proteinate stain; X 23,600.) Fig. 4. Micrograph showing conjunctival fibroblast with glycogen-filled lysosomes (large arrow), Note intermediate stage of lysosomal involvement (small arrows). G, Glycogen; IV, nucleus. (Silver proteinate stain; X9199.) azure H-methylene blue 24 or toluidine blue. Thin sections were stained with uranyl and lead. 25 To enhance ultrastructural localization of glycogen, a modification of the periodic acid-thiocarbohydrazide-silver proteinate reaction was performed, 2 *" in which thin sections were supported on gold grids and treated for 20 min with 1% periodic acid, after which time they were floated on the thiocarbohydrazide reagent for 1, 12, 24, 48, and 72 hr. This was followed by staining with silver proteinate for 30 min. Results Light microscopy. Generalized light histopathologic study revealed development of the eye compatible with 16 week gestation. PAS-positive granules were digested by diastase in sections of extraocular muscle. They were thus identified as glycogen. Electron microscopy. Glycogen particles (/3-type) were observed by routine contrast stains in almost all of the ocular tissue examined (Figs. 1, 5, 8, and 10), including conjunctiva, cornea, iris, retina, choroid, and extraocular muscle. The affinity of the particles for silver proteinate confirmed their identification as glycogen. The glycogen granules were found primarily in membrane- delimited, vacuolar inclusion bodies of various dimensions (from 0.25 to 2 fjun or more in length) (Figs. 3, 6, 7, and 10). In addition, large amounts of glycogen were dispersed cy- Fig. 5. Micrograph showing rhabdomyoblast of developing extraocular muscle. There are massive accumulations of cytoplasmic glycogen interspersed among the fibrillar bundles. Arrows show lysosomes that contain glycogen particles. A', Nucleus. (Uranyl-lead stain; X3682.) toplasmically (Figs. 1, 2, 5, and 8). The fine structure of the fetal ocular tissue appeared normal in other respects. Some of the inclusion bodies were only partially filled with glycogen, the remainder appearing homogeneously electron-dense (Figs. 2 and 4). In many areas the membrane-delimited saccules were confluent, having barely discernible boundaries (Fig. 7). Conjunctival basal
4 28 Pokorny et al. Inoest. Ophthalmol. Vis. Set. January 1982 r *«* Fig. 6. Micrograph showing rhabdomyoblast of developing extraocular muscle. Massive lysosomal and cytoplasmic deposits of glycogen are present. Large arrow indicates areas of possible rupture of lysosomal membrane leading to confluence of inclusions and dense deposits of glycogen granules. G, Glycogen; N, nucleus; f, fibrils. (Uranyl-lead stain; X6879.) epithelium and fibroblasts showed marked involvement (Figs. 1 and 4), as did comeal epithelium and keratocytes in the stroma and rhabdomyoblasts of developing extraocular muscle (Figs. 5 and 6). Extraocular muscle showed the greatest concentration of membrane-bound, glycogen-filled inclusions. Cytoplasmic deposits were also found between the latticelike myofibrils. Some cell types in extraocular muscle were difficult to identify because of massive glycogen accumulation and confluence of the inclusion bodies (Fig. 7). Retina displayed glycogen storage, with the remarkable exception of retinal pigment epithelium (Figs. 9 and 10). Developing iris was involved in deposition, although no inclusions were seen in iris pigment epithelium. Capillary endothelium and nerve of various tissues showed some involvement, with sparser involvement of nerve. Discussion Prenatal diagnosis, through amniocentesis and enzyme analysis of cultured amniotic cells, now permits the early detection of a number of inborn errors of metabolism. l2 ~ 14< 27 ~ 29 In the present case the total absence of acid a- 1,4-glucosidase activity in cultured amniotic Fig. 7. Micrograph showing cell from developing extraocular muscle. The deposition of glycogen is so excessive that the whole cell isfilled.only a rim of cytoplasm is visible at the periphery of the cell. (Silver proteinate stain; X4425.) cells was diagnostic of Pompe's disease, and the pregnancy was terminated. Light and electron microscopic histopathologic findings confirmed the diagnosis. Glycogen deposition, both within membrane-delimited vacuoles and free in the cytoplasm, was consistent with ultrastructural studies on cultured amniotic cells in Pompe's disease. 12 ' 13 The positive reaction to silver proteinate, which allows ultrastructural visualization of aldehyde-containing polysaccharides, confirmed the nature of the deposits. The membrane-bound inclusions were typical of secondary lysosomes or residual bodies and were similar to the lesions usually seen in Pompe's. 2 ' 5l 13 Their appearance in virtually all of the tissue that was examined indicated widespread storage, even at so early a gestational stage. Although fetal tissue is normally glycogen-rich, the carbohydrate is typically found as free particles throughout the cytoplasm. In Pompe's disease, glycogen is characteristically localized within lysosomes; it is also found in unusually large amounts in the cytoplasm. 5-6
5 Volume 22 Number 1 Ultrastructure of eye in Pompe's disease 29 Fig. 8. Micrograph showing choroidal fibroblasts extensively involved in glycogen deposition. Note large membrane-bound lysosome with glycogen particles. One cell appears to be in an early stage of necrosis. (Uranyl-lead stain; X5162.) Extraocular muscle was the most heavily involved tissue, as indicated by the enormity and confluence of the glycogen-engorged lysosomes. Comparison of random electron micrographs of this fetus with those reported by Libert et al. 16 indicates as much, if not more, glycogen in this 16 week fetus as that in the 22 week one. Skeletal muscle is usually heavily involved in all forms of the disease, 3 ' llj 1G ' 30 and the massive deposits seen in extraocular muscle here may be responsible for the apparent rupture of lysosomal membranes, resulting in large, confluent, glycogen-engorged bodies. Massive accumulations between myofibrils may be the result of lysosomal saturation, leaving no place for excess glycoqen to be stored. Glycogen-degrading enzymes in the cytoplasm are apparently not sufficient to handle the breakdown of excess glycogen so displaced. Accumulations of excess glycogen have been noted in skeletal muscle in the juvenile 21 and fetal 16 forms. With the exception of pigment epithelium Fig. 9. Micrograph showing developing retinal pigment epithelium with melanin (m). No glycogen deposition is seen. Choroidal fibroblasts show extensive involvement. (Uranyl-lead stain; X7965.)- of iris and retina, all of the tissues examined, including conjunctiva, cornea, iris, extraocular muscle, retina, and choroid, had massive glycogen deposition. The lack of deposition in retinal pigment epithelium is in agreement with the results of Libert et al. 16 in their report of a 22 week fetus and with the results of Goebel et al., 20 who reported preferential involvement of photoreceptor inner segments and inner granular ganglionic cells in a 9-month-old infant with the disease. The lack of glycogen inclusions in iris pigment epithelium is a new finding. The reasons for the apparent absence of glycogen in these pigment epithelia (iris and retina) are unclear and are perhaps caused by some functional difference in lysosomal enzymes of pigment epithelia over other cell types. The involvement of retinal pigment epithelium in phagocytosis may have to do with its lack of glycogen storage. Perhaps the turnover is so rapid in pigment epithelia that the substrate simply does not have time to accumulate. Or it may
6 30 Pokorny et al. Invest, Ophthalmol. Vis. Set. January 1982 indicative of Pompe's disease are already formed at this early stage of development, as shown by the extensive involvement of ocular tissue. The marked involvement of the conjunctiva confirms the value of conjunctival biopsy in the diagnosis of inborn errors of metabolism. Fig. 10. Micrograph showing retina in region of outer limiting membrane. Arrows indicate glycogen-filled lysosomes. (Silver proteinate stain; X9017.) simply be caused by an as yet undeveloped system. The observation of partially filled lysosomes suggests intermediate stages in glycogen segregation within the enzyme-deficient lysosomes. Although acid a-glucosidase normally hydrolyses lysosomally trapped glycogen into oligosaccharides and glucose, 31 no account can thus far be made for the fact that greater-than-normal amounts of glycogen are disseminated throughout the cytoplasm in this disease. Studies on muscle 15 led to the speculation that this was due to the fact that myofibrillar glycogen amassed early in the disease process, penetrating the lysosomes later on. This would explain the presence of some cytoplasmic glycogen. Further overdistension of glycogen-engorged vacuoles could cause disruption of the lysosomes, 9 providing another mechanism for the accumulation of glycogen in the cytoplasmic pool. The accumulation of free cytoplasmic glycogen has also led to speculations that an enzyme other than acid a-l,4-glucosidase is involved, and some investigators presented evidence of decreased neutral maltase activity in the infantile :ji ~ 33 and late onset 33 forms. Abnormal, glycogen-engorged lysosomes We thank Laurie Raisher, Joseph Suhan, and Michalina Lokietko for their excellent and cheerful technical assistance, and we gratefully acknowledge Stem ma Askinazi for typing the manuscript, REFERENCES 1. Hers HG: a-glucosidase deficiency in generalized glycogen-storage disease (Pompe's disease). Biochem J 86:11, Baudhin P, Hers HC, and Loeb H: An electron microscopic and biochemical study of type II glycogenosis. Lab Invest 13:1139, Garancis JC: Type II glycogenosis, biochemical and electron microscopic study. Am J Med 44:289, Hug G: Nonbilirubin genetic disorders of the liver. Intl Acad Pathol Monogr 13:21, Hers HG and de Barsy T: Type II glycogenosis (acid maltase deficiency). In Lysosomes and Storage Diseases, Hers HG and Van Hoof F, editors. New York, 1973, Academic Press, Inc. 6. Hug G, Garancis JC, Schubert WK, and Kaplan S: Glycogen storage disease, types II, III, VIII, and IX. Am J Dis Child 111:457, Martin JJ, de Barsy T, Van Hoof F, and Palladini G: Pompe's disease: an inborn lysosomal disorder with storage of glycogen. Acta Neuropathol 23:229, Howell RR: The glycogen storage diseases. In The Metabolic Basis of Inherited Disease, Stanbury JB, Wyngaarden JB, and Fredrickson DS, editors. New York, 1978, McGraw-Hill Book Co. 9. Hudgson P, Gardner-Medwin D, Worsfold M, Pennington RJT, and Walton JN: Adult myopathy From glycogen storage disease due to acid maltase deficiency. Brain 91:435, Engel AG: Acid maltase deficiency in four cases of a syndrome which may mimic muscular dystrophy or other myopathies. Brain 93:599, Engel AG, Gomez MR, Seybold ME, and Lambert EH: The spectrum and diagnosis of acid maltase deficiency, Neurology 23:95, Nadler HL and Messina AM: In-utero detection of type II glycogenosis (Pompe's disease). Lancet 2:1277, Hug G, Schubert WK, and Soukup S: Prenatal diagnosis of type II glycogenosis. Lancet 1:1002, Hug G: Enzyme therapy and prenatal diagnosis in glycogenosis type II. Am J Dis Child 128:607, Cardiff RD: A histochemical and electron microscopic study of skeletal muscle in a case of Pompe's disease (glycogenosis II). Pediatrics 37:249, 1966.
7 Volume 22 Number 1 Ultrastructure of eye in Pompe's disease Libert J, Matrin JJ, Ceuterick C, and Danis P: Ocular ultrastructural study in a fetus with type II glycogenosis. Br J Ophthalmol 61:476, Pellegrini G, Mosca G, and Cerri C: Pompe's disease: ultrastructural alterations of muscle tissue in parents. Acta Neurol Scand 57:216, Toussaint D and Danis P: Ocular histopathology in generalized glycogenosis. Arch Ophthalmol 73:342, Goebel HH, Zeman W, Kohlschutter A, Pilz H, and Koppang N: Ultrastructure of the retina in lysosomal disorders. Doc Ophthalmol 17:369, Goebel HH, Kohlschutter A, and Pilz H: Ultrastructural observations on the retina in type II glycogenosis (Pompe's disease). Ophthalmologica 176:61, Smith RS and Reinecke RD: Electron microscopy of ocular muscle in type II glycogenosis (Pompe's disease). Am J Ophthalmol 73:965, Pokorny KS, Ritch R, and Friedman AH: A trialdehyde fixative for routine ophthalmic pathology. (In preparation.) 23. Ritch R and Philpott CW: Repeating particles associated with an ion-transporting membrane. Exp Cell Res 55:7, Richardson KC, Jarett L, and Finke EH: Embedding in epoxy resins for ultra thin sectioning in electron microscopy. Stain Technol 35:313, Venable J and Coggeshall RJ: A simple new lead stain for electron microscopy. J Cell Biol 25:407, Thiery J-P: Mise en evidence des polysaccharides sur coupes fines en microscopie electronique. J Microscopie 6:997, Schneider EL, Ellis VVG, Brady RO, McCulloch JR, and Epstein CJ: Prenatal Niemann-Pick disease: biochemical and histologic examination of a 19- gestational week fetus. Pediatr Res 6:720, Howes EL, Wood IS, Golbus M, and Hogan ML: Ocular pathology of infantile Niemann-Pick disease. Arch Ophthalmol 93:494, Adachi M, Schneck L, and Volk BW: Ultrastructural studies of eight cases of fetal Tay-Sachs disease. Lab Invest 30:102, Martin JJ, de Barsy T, de Schrijver F, Leroy JG, and Palladini G: Acid maltase deficiency (type II glycogenosis): morphological and biochemical study of a childhood phenotype. J Neurol Sci 30:155, Hers HG: The concept of inborn lysosomal disease. In Lysosomes and storage disease, Hers HG and Van Hoof F, editors. New York, 1973, Academic Press, Inc., pp Angelini C and Engel AG: Comparative study of acid maltase deficiency: biochemical differences between infantile, childhood, and adult types. Arch Neurol 26:344, Mehler M and DiMauro S: Residual acid maltase activity in late-onset acid maltase deficiency. Neurology 27:178, 1977.
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British Journal of Ophthalmology, 1977, 61, 476-482 Ocular ultrastructural study in a fetus with type II glycogenosis J. LIBERT,1 J.-J. MARTIN,2 C. CEUTERICK,2 AND P. DANIS' From the Department of Ophthalmology,
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