Summary
Impairment of skeletal muscle function is the common feature of distinct clinical forms of glycogenosis type II. In the present study, muscle cultures from different patients were used to investigate the cause of clinical heterogeneity and the feasibility of enzyme replacement therapy. The activity of acid α-glucosidase appears to be the primary factor in determining the extent of lysosomal glycogen storage in muscle, and thereby the clinical severity of the disease. Neutral α-glucosidases do not seem influencial. Correction of the enzymatic defect was achieved in skeletal muscle cultures from patients by administration of a “high-uptake” form of acid α-glucosidase, purified from human urine. The enzyme reaches the lysosomes, including the glycogen storage vacuoles, and the lysosomal glycogen content is reduced to control level. In normal muscle cells 20% of the total cellular glycogen pool is segregated in lysosomal compartments. This percentage is higher than in fibroblasts, which may partly explain why muscles are more prone to store glycogen. The relevance of this study for enzyme therapy is discussed.
Similar content being viewed by others
References
Angelini C, Engel AG (1972) Comparative study of acid maltase deficiency. Arch Neurol 26:344–349
Askanas V, Engel WK, DiMauro S, Brooks BR, Mehler M (1976) Adult-onset acid maltase deficiency. Morphological and biochemical abnormalities reproduced in cultured muscle. N Engl J Med 294:573–578
Barranger JA (1984) Marrow transplantation in genetic disease. N Engl J Med 311:1629–1631
Bolhuis PA, De Zwart HJD, Ponne NJ, De Jong JMBV (1985) Free-energy carriers in cultured muscle cells. Muscle Nerve 8:22–26
De Bruijn WC (1973) Glycogen, its chemistry and morphologic appearance in the electron microscope. A modified OsO4 fixative which selectively contrasts glycogen. J Ultrastruct Res 42:29–50
Desnick RJ (ed) (1980) Enzyme therapy in genetic diseases: 2. Liss, New York
DiMarco PN, Howell JMcC, Dorling PR (1985) Bovine generalised glycogenosis type II. Uptake of lysosomal α-glucosidase by cultured skeletal muscle and reversal of glycogen accumulation. FEBS Lett 190:301–304
Galjaard H (1980) Genetic metabolic diseases: early diagnosis and prenatal analysis. Elsevier/North Holland, Amsterdam New York, pp 809–827
Griffin JL (1984) Infantile acid maltase deficiency. Muscle fiber destruction after lysosomal rupture. Virchows Arch B 45:23–36
Hers HG, De Barsy T (1973) Type II Glycogenosis (acid maltase deficiency). In: Hers HG, Van Hoof F (eds) Lysosomes and storage diseases. Academic Press, New York London
Howell RR, Williams JC (1983) Disorders of lysosomal enzymes. In: Stanbury JB, Wyngaarden JB, Fredrickson DS, Goldstein JL, Brown MS (eds) The metabolic basis of inherited disease. McGraw-Hill, New York
Hug G, Schubert WK (1967) Lysosomes in type II glycogenosis. Changes during administration of extract from Aspergillus niger. J Cell Biol 35:C1–6
Kaplan A, Achord DT, Sly WS (1977) Phosphohexosyl components of a lysosomal enzyme are recognized by pinocytosis receptors on human fibroblasts. Proc Natl Acad Sci USA 74:2026–2030
Koster JF, Slee RG, Hulsman WC (1972) The use of leucocytes as an aid in the diagnosis of a variant of glycogen storage disease type II (Pompe's disease). Eur J Clin Invest 2:467–471
Krivit W, Paul NW (eds) (1986) Bone marrow transplantation for treatment of lysosomal storage diseases. Liss, New York
Lowry OH, Rosebrough NJ, Farr Al, Randall RJ (1951) Protein measurement with the folin phenol reagent. J Biol Chem 193:265–275
Mehler M, DiMauro S (1977) Residual acid maltase activity in late-onset acid maltase deficiency. Neurology 27:178–184
Miranda AF, Shanske S, Hays AP, DiMauro S (1985) Immunocytochemical analysis of normal and acid maltase-deficient muscle cultures. Arch Neurol 42:371–373
Ninomiya N, Matsuda I, Matsuoka T, Iwamasa T, Nonaka I (1984) Demonstration of acid α-glucosidase in different types of Pompe disease by use of an immunochemical method. J Neurol Sci 66:129–139
Oude Elferink RPJ, Brouwer-Kelder EM, Surya I, Strijland A, Kroos M, Reuser AJJ, Tager JM (1984) Isolation and characterization of a precursor form of lysosomal α-glucosidase from human urine. Eur J Biochem 139:489–495
Oude Elferink RPJ, Strijland A, Surya I, Brouwer-Kelder EM, Kroos M, Hilkens J, Hilgers J, Reuser AJJ, Tager JM (1984) Use of a monoclonal antibody to distinguish between precursor and mature forms of human lysosomal α-glucosidase. Eur J Biochem 139:497–502
Oude Elferink RPJ, Van Doorn-Van Wakeren J, Hendriks T, Strijland A, Tager JM (1986) Transport and processing of endocytosed lysosomal α-glucosidase in cultured human skin fibroblasts. Eur J Biochem 158:339–444
Parkman R (1986) The application of bone marrow transplantation to the treatment of genetic diseases. Science 232:1373–1378
Reuser AJJ, Kroos MA, Ponne NJ, Wolterman RA, Loonen MCB, Busch HFM, Visser WJ, Bolhuis PA (1984) Uptake and stability of human and bovine acid α-glucosidase in cultured fibroblasts and skeletal muscle cells from glycogenosis type II patients. Exp Cell Res 155:178–189
Reuser AJJ, Kroos M, Oude Elferink RPJ, Tager JM (1985) Defects in synthesis, phosphorylation and maturation of acid α-glucosidase in glycogenosis type II. J Biol Chem 260:8336–8341
Reuser AJJ, Kroos M, Willemsen R, Swallow D, Tager JM, Galjaard H (1987) Clinical diversity in Glycogenosis type II. Biosynthesis and in situ localization of acid α-glucosidase in mutant fibroblasts. J Clin Invest 79:1689–1699
Udenfriend S, Stein S, Bohlen P, Dairman W, Leimgruber W, Weigele M (1972) Fluorescamine: a reagent for assay of amino acids, peptides, proteins, and primary amines in the picomole range. Science 178:871–872
Van der Ploeg AT, Kroos M, Van Dongen JM, Visser WJ, Bolhuis PA, Loonen MCB, Reuser AJJ (1987) Breakdown of lysosomal glycogen in cultured fibroblasts from glycogenosis type II patients after uptake of acid α-glucosidase. J Neurol Sci 79:327–336
Van Dongen JM, Barneveld RA, Geuze HJ, Galjaard H (1984) Immunocytochemistry of lysosomal hydrolases and their precursor forms in normal and mutant human cells. Histochem J 16:941–954
Watson JG, Gardner-Medwin D, Goldfinch ME, Pearson ADJ (1986) Bone marrow transplantation for glycogen storage disease type II (Pompe's disease). N Engl J Med 314:385
Yaffe D (1968) Retention of differentiation potentialities during prolonged cultivation of myogenic cells. Proc Natl Acad Sci USA 61:477–483
Yasin R, Van Beers G, Nurse KCE, Ali-Ani S, Landon DN, Thompson EJ (1977) A quantitative technique for growing human adult skeletal muscle in culture starting from mononucleated cells. J Neurol Sci 32:347–360
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
van der Ploeg, A.T., Bolhuis, P.A., Wolterman, R.A. et al. Prospect for enzyme therapy in glycogenosis II variants: a study on cultured muscle cells. J Neurol 235, 392–396 (1988). https://doi.org/10.1007/BF00314479
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF00314479