Summary
Lysosomal diseases result from deficiency of one of the many enzymes involved in the normal, step-wise breakdown of macromolecules. Studies in vitro have shown that cells from enzyme-deficient patients can be corrected by an exogenous supply of the missing enzyme. This occurs by receptor-mediated endocytosis of normal enzyme added to tissue culture medium and also by direct transfer from normal leukocytes during cell-to-cell contact. Immunohistochemical analysis has revealed that these processes have similar pathways of intracellular transport of the acquired enzymes, which ultimately reach mature lysosomes in the recipient cells. Moreover, recent studies suggest that both mechanisms are important in the therapy of lysosomal storage diseases by bone marrow transplantation. Advances in gene technology are likely to improve the successful treatment of these disorders, by facilitating the large scale production of clinically effective proteins and also by enabling the stable and safe introduction of normal lysosomal genes into cells of affected patients.
Similar content being viewed by others
References
Abraham, D., Muir, H., Olsen, I. & Winchester, B. (1985) Direct enzyme transfer from lymphocytes corrects a lysosomal storage disease. Biochem. Biophys. Res. Commun. 129, 417–25.
Abraham, D., Muir, H., Winchester, B. & Olsen, I. (1988) Lymphocytes transfer only the lysosomal form of α-d-mannosidase during cell-to-cell contact. Exp. Cell Res. 175, 158–68.
Abraham, D., Bokth, S., Bou-Gharios, G., Beauchamp, J. & Olsen, I. (1990) Interactions between lymphocytes and dermal fibroblasts: an in vitro model of cutaneous lymphocyte trafficking. Exp. Cell Res. 190, 118–26.
Adams, D. O., Johnson, W. J. & Marino, P. A. (1982) Mechanisms of target recognition and destruction in macrophagemediated tumour cytotoxicity. Fed. Proc. 41, 2212–21.
Adinolfi, M., Akle, C., Mccoll, I., Fensom, A. H., Tansley, L., Connolly, P., Hsi, B.-L., Faulk, W. P., Travers, P. & Bodmer, W. F. (1982) Expression of HLA antigens B2 microglobulin and enzymes by human amniotic epithelial cells. Nature 295, 325–27.
Akle, C. A., Adinolfi, M., Welsh, K. I., Leibowitz, S. & Mccoll, I. (1981) Immunogenicity of human amniotic epithelial cells after transplantation into volunteers. Lancet ii, 1003–5.
Andre, P., Benoliel, A.-M., Capo, C., Foa, C., Buferne, M., Boyer, C., Schmitt-Verhulst, A.-M. & Bongrand, P. (1990) Use of conjugates made between a cytolytic T cell clone and target cells to study the redistribution of membrane molecules in cell contact areas. J. Cell Sci. 97, 335–47.
Bach, G., Bargal, R. & Cantz, M. (1979) I-cell disease: deficiency of extracellular hydrolase phosphorylation. Biochem. Biophys. Res. Commun. 91, 976–81.
Barkla, D. H., Whitehead, R. H., Foster, H. & Tutton, P. H. (1988) Tuft (caveolated) cells in two human colon carcinoma cell lines. Am. J. Pathol. 132, 521–5.
Barr, E. & Leiden, J. M. (1991) Systemic delivery of recombinant proteins by genetically modified myoblasts. Science 254, 1507–9.
Barranger, J. A. & Ginns, E. I. (1989) Glucosylceramide lipidoses: Gaucher disease. In The metabolic basis of inherited disease (edited by Scriver, C. R., Beaudet, A. L., Sly, W. S. & Valle, D.) pp. 1677–89. New York: Mc-Graw-Hill.
Barton, N. W., Brady, R. O., Dambrosia, J. M., Doppelt, S. H., Hill, S. C., Holder, C. A., Mankin, H. J., Murray, G. J., Zirzow, G. C. & Parker, R. I. (1992) Dose-dependent responses to macrophage-targeted glucocerebrosidase in a child with Gaucher disease. J. Ped. 120, 277–80.
Beauchamp, J. R., Abraham, D., Bou-Gharios, G., Partridge, T. A. & Olsen, I. (1992) Expression and function of heterotypic adhesion molecules during differentiation of human skeletal muscle. Am. J. Path. 140, 387–401.
Birkenmeier, E. H., Baker, J. E., Volger, C. A., Kyle, J. W., Sly, W. S., Gwynn, B., Levy, B. & Pegors, C. (1991) Increased life span and correction of metabolic defects in murine mucopolysaccharidosis type VII after syngeneic bone marrow transplantation. Blood 78, 3081–92.
Boggs, S. S. (1990) Targeted gene modification for gene therapy of stem cells. Int. J. Cell Clon. 8, 80–96.
Bou-Gharios, G., Moss, J., Abraham, D., Partridge, T. & Olsen, I. (1988) Ultrastructural studies of a lysosomal enzyme during lymphocyte activation. Br. J. Exp. Pathol. 69, 661–70.
Bou-Gharios, G., Moss, J. & Olsen, I. (1991a) Localization of lysosomal antigens in activated T-lymphocytes. Histochem. J. 23, 474–82.
Bou-Gharios, G., Moss, J., Partridge, T., Abraham, D. & Olsen, I. (1991b) Contact-dependent transfer of a lysosomal enzyme from lymphocytes to fibroblasts. J. Cell Sci. 100, 443–9.
Bou-Gharios, G., Adams, G., Pace, P., Warden, P. & Olsen, I. (1993) Correction of a genetic deficiency by contact-mediated lysosomal enzyme transfer from bone marrow cells in vivo. Transplantation (in press).
Brown, J. A., Novak, E. K. & Swank, R. T. (1985) Effects of ammonia on processing and secretion of precursor and mature lysosomal ensyme from macrophages of normal and pale ear mice: evidence for two distinct pathways. J. Cell Biol. 100, 1894–904.
Bucana, C., Hoyer, L. C., Hobbs, B., Bressman, S., Mcdaniel, M. & Hannan, M. G. (1976) Morphological evidence for the translocation of lysosomal organelles from cytotoxic macrophages into the cytoplasm of tumour target cells. Cancer Res. 36, 4444–58.
Chao, H. H.-J., Waheed, A., Pohlmann, R., Hille, A. & VonFigura, K. (1990) Mannose 6-phosphate receptor dependent secretion of lysosomal enzymes. EMBO J. 9, 3507–13.
Chowdhury, J. R., Grossman, M., Gupta, S., Chowdhury, N. R., Baker, J. R. & Wilson, J. M. (1991) Long-term improvement of hypercholesterolemia after ex vivo gene therapy in LDL-deficient rabbits. Science 254, 1802–5.
Correll, P. H., Fink, J. K., Brady, R. O., Perry, L. K. & Karlsson, S. (1989) Production of human glucocerebrosidase in mice after retroviral gene transfer into multipotential hematopoietic progenitor cells. Proc. Natl Acad. Sci. USA 86, 8912–6.
Correll, P. H., Kew, Y., Perry, L. K., Brady, R. O., Fink, J. K. & Karlsson, S. (1990) Expression of human glucocerebrosidase in long-term reconstituted mice following retroviralmediated gene transfer into hematopoietic stem cells. Hum. Gene Ther. 1, 277–87.
Crawfurd, M. D., Gibbs, D. A. & Watts, R. W. E. (eds) (1982) Advances in the Treatment of Inborn Errors of Metabolism. Chichester: John Wiley.
Dean, M. F. & Martin, J. C. (1988) Intracellular localization of β-glucuronidase in fibroblasts after direct transfer from macrophages. Biochem. J. 256, 335–41.
Dean, M. F., Muir, H. & Benson, P. (1973) Mobilisation of glycosaminoglycans by plasma infusion in mucopolysaccharidosis type III - two types of response. Nature 243, 143–6.
Dean, M. F., Muir, H., Benson, P. F., Button, L. R., Boylston, A. & Mowbray, J. (1976) Enzyme replacement therapy by fibroblast transplantation in a case of Hunter syndrome. Nature 261, 323–5.
Dean, M. F., Stevens, R. L., Muir, H., Benson, P. F., Button, L. R., Anderson, R. L., Boylston, A. & Mowbray, J. (1979) Enzyme replacement therapy by fibroblast transplantation. Long-term biochemical study in three cases of Hunter's syndrome. J. Clin. Invest. 63, 138–45.
Dean, M. F., Mcnamara, A. & Jenne, B. M. (1985) Direct transfer of β-glucuronidase from mouse macrophages to other type of cell. J. Cell Sci. 79, 137–49.
Dean, M. F., Cooper, J. A. & Stahl, P. (1988) Cell contact and direct transfer between co-cultured macrophages and fibroblasts. J. Leuk. Biol. 43, 539–46.
Dean, M. F., Rodman, J., Levy, M. & Stahl, P. (1991) Contact formation and transfer of mannose BSA gold from macrophages to cultured fibroblasts. Exp. Cell Res. 192, 536–42.
Dennert, G., Kupfer, A., Anderson, C. & Singer, S. (1986) Reorientation of the Golgi apparatus and the microtubule organizing centre: Is it a means to polarize cell-mediated cytotoxicity? In Mechanisms of Cell-mediated Cytotoxicity II (edited by Henkart, P. & Martz, E.) pp. 83–117. New York: Plenum Press.
Desnick, R. J. (ed) (1980) Enzyme Therapy in Genetic Diseases: 2. New York: Alan R. Liss.
Dhawan, J., Pan, L. C., Pavlath, G. K., Travis, M. A., Lanctot, A. M. & Blau, H. M. (1991) Systemic delivery of human growth hormone by injection of genetically engineered myoblasts. Science 254, 1509–12.
DiFerranti, R., Nichols, B. L., Donnelly, P. V., Neri, G., Hrgocic, R. & Berglund, R. K. (1971) Induced degradation of glycosaminoglycans in Hurler's and Hunter's syndrome by plasma infusion. Proc. Natl Acad. Sci. USA 68, 303–7.
DiFerranti, N., Nichols, B. L., Knudson, A. G., Mccredie, K. B., Singh, J. & Donnelly, P. V. (1973) Mucopolysaccharide-storage Diseases: Corrective Activity of Normal Human Serum and Lymphocytes. New York: Alan R. Liss.
Dustin, M. L. & Springer, T. A. (1991) Role of lymphocyte adhesion receptors in transient interactions and cell locomotion. Annu. Rev. Immunol. 9, 27–66.
Edelman, G. M. & Crossin, K. L. (1991) Cell adhesion molecules: implications for a molecular histology. Annu. Rev. Biochem. 60, 155–90.
Feder, N. (1976) Solitary cells and enzyme exchange in tetraparental mice. Nature 263, 67–9.
Furbish, F. S., Steer, C. J., Barranger, J. A., Jones, E. A. & Brady, R. O. (1978) The uptake of native and desialylated glucocerebrosidase by rat hepatocytes and Kuffer cells. Biochem. Biophys. Res. Commun. 81, 1047–53.
Furbish, F. S., Oliver, K. L., Zirzow, G. C., Brady, R. O. & Barranger, J. A. (1984) In The Molecular Basis of Lysosomal Storage Disorders (edited by Barranger, J. A. & Brady, R. O.) pp. 219–32. Orlando, FL: Academic Press.
Gasper, P. W., Thrall, M. A., Wenger, D. A., Macy, D. W., Ham, L., Dornsife, R. E., Mcbiles, K., Quackenbush, S. L., Kesel, M. L., Gillette, E. L. & Hoover, E. A. (1984) Correction of feline arylsulphatase B deficiency (molysaccharidosis VI) by bone marrow transplanation. Nature 312, 467–9.
Geuze, H. & Morre, D. (1991) Trans-Golgi reticulum. J. Electron Microsc. 17, 24–34.
Geuze, H. J., Stoorvogel, W., Strous, G. J., Slot, J. W., Bleekemolen, J. E. & Mellman, I. (1988) Sorting of mannose 6-phosphate receptors and lysosomal membrane proteins in endocytic vesicles. J. Cell Biol. 107, 2491–501.
Ginsel, L. A. & Fransen, J. A. (1991) Mannose 6-phosphate receptor independent targeting of lysosomal enzymes (a mini-review). Cell Biol. Int. Rep. 15, 1167–73.
Griffiths, G. & Simons, K. (1986) The trans Golgi network: sorting at the exit site of the Golgi complex. Science 234, 438–43.
Griffiths, G., Hoflack, B., Simons, K., Mellman, I. & Kornfeld, S. (1988) The mannose 6-phosphate receptor and the biogenesis of lysosomes. Cell 52, 329–41.
Groth, C. G. & Ringden, O. (1984) Transplantation in relation to the treatment of inherited diseases. Transplantation 38, 319–27.
Helenius, A., Mellman, I., Wall, D. & Hubbard, A. (1983) Endosomes. TIBS 8, 245–50.
Henkart, P. A. (1985) Mechanism of lymphocyte-mediated cytotoxicity. Annu. Rev. Immunol. 3, 31–58.
Heut, C., Ash, J. & Singer, S. (1980) The antibody-induced clustering and endocytosis of HLA antigens on clustered human fibroblasts. Cell 21, 429–38.
Ho, M. W. (1973) Identity of ‘acid’ β-glucosidase and glucocere-brosidase in human spleen. Biochem. J. 136, 721–9.
Hobbs, J. R. (1985) Correction of 34 genetic diseases by displacement bone marrow transplantation. Plasma Ther. Transfus. Technol. 6, 221–46.
Hoogerbrugge, P. M., Poorthuis, B. J., Mulder, A. H., Wagemaker, G., Dooren, L. J., Vossen, J. M. & Van-Bekkum, D. W. (1987) Correction of lysosomal enzyme deficiency in various organs of β-glucuronidase-deficient mice by allogeneic bone marrow transplantation. Transplantation 43, 609–14.
Hugh-Jones, K., Hobbs, J., Chambers, D., White, S., Byrom, N., Williamson, S., Barrett, J., Kristin, H. & Patrick, D. (1984) Bone marrow transplantation in mucopolysaccharidoses. In Molecular Basis of Lysosomal Storage Disorders (edited by Barranger, J. D. & Brady, R. O.) pp. 411–28. New York: Academic Press.
Jenkins, H. G., Martin, J. & Dean, M. F. (1988) Receptor-mediated uptake of β-glucuronidase into primary astrocytes and C6 glioma cells from rat brain. Brain Res. 462, 265–74.
Jolly, R. D., Thompson, K. G., Murphy, C. E., Manktelow, B. W., Bruere, A. N. & Winchester, B. G. (1976) Enzyme replacement therapy - an experiment of nature in a chimeric mannosidosis calf. Pediat. Res. 10, 219–24.
Kaplan, J. (1976) Cell contact induces an increase in pinocytotic rate in cultured epithelial. Nature 263, 596–7.
Kornfeld, S. (1986) Trafficking of lysosomal enzymes in normal and disease states. J. Clin. Invest. 77, 1–6.
Kornfeld, S. (1987) Trafficking of lysosomal enzymes. Faseb. J. 1, 462–8.
Kornfeld, S. & Mellman, I. (1989) The biogenesis of lysosomes. Ann. Rev. Cell Biol. 5, 483–525.
Krivit, W. & Paul, N. W. (eds) (1986) Bone Marrow Transplantation for Treatment of Lysosomal Storage Diseases. Birth Defects, Original Series. New York: Alan R. Liss.
Krivit, W., Whitley, C. B., Chang, P. N., Shapiro, E. & Belani, K. G. (1990) In Bone Marrow Transplantation in Children (edited by Johnson, F.L. & Pochedly, C.) pp. 261–87. New York: Raven Press.
Lehn, P. M. (1990) Gene therapy using bone marrow transplantation: a 1990 update. Bone. Marr. Trans. 5, 287–93.
Lightbody, J., Wiesmann, U., Hadorn, B., Herschkowitz, Hadorn, B. & Herschkowitz, N. (1971) I-cell disease: multiple lysosomal-enzyme defect. Lancet i, 451–6.
Lin, Berzofsky, J. A. & Delovitch, T. L. (1988) Ultrastructural study of internalization and recycling of antigen by antigen presenting cells. J. Mol. Cell Immunol. 3, 321–43.
Luciano, L. & Reale, E. (1979) A new morphological aspect of the brush cells of the mouse gall bladder. Cell Tissue Res. 251, 37–44.
Mckinnon, K. P., Dunlevy, J. R., Dawson, J. R. & Argon, Y. (1988) Cell-mediated cytotoxicity and the reorientation of effector cell granules towards the target cell are inhibited by the protonophore carbonylcyanide m-chlorophenylhydrazone. Hum. Immunol. 22, 81–95.
Mcnamara, A., Jenne, B. M. & Dean, M. F. (1985) Fibroblasts acquire β-glucuronidase by both direct and indirect transfer during co-culture with macrophages. Exp. Cell Res. 160, 150–7.
Matovcik, L. M., Goodhouse, J. & Farquhar, M. G. (1990) The recycling itinerary of the 46 kDa mannose 6-phosphate receptor - Golgi to late endosomes - coincides with that of the 215 kDa M6PR. Eur. J. Cell Biol. 53, 203–11.
Merion, M. & Sly, W. S. (1983) The role of intermediate vesicles in the adsorptive endocytosis and transport of ligand to lysosomes by human fibroblasts. J. Cell Biol. 96, 644–50.
Miller, A. D. (1992) Human gene therapy comes of age. Nature 357, 455–60.
Montesano, R., Roth, J., Robert, A. & Orci, L. (1982) Noncoated membrane invaginations are involved in binding and internalization of cholera and tetanus toxins. Nature 296, 651–3.
Morgan, J. E., Coulton, G. R. & Partridge, T. A. (1987) Muscle precursor cells invade and repopulate freeze-killed muscles. J. Mus. Res. Cell Motil. 8, 386–96.
Nabeyama, A. & Leblond, C. P. (1974) ‘Caveolated cells’ characterized by deep surface invaginations and abundant filaments in mouse gastro-intestinal epithelia. Am. J. Anat. 140, 147–65.
Neufeld, E. F. (1980) The uptake of enzymes into lysosomes: an overview. In Enzyme Therapy in Genetic Diseases: 2 (edited by Desnick, R.J.) pp. 77–84. New York: Alan R. Liss.
Neufeld, E. F. (1991) Lysosomal storage diseases. Annu. Rev. Biochem. 60, 257–80.
Neufeld, E., Lim, T. & Sharpio, L. (1976) Annu. Rev. Biochem. 44, 356–7.
Nickoloff, B. J., Griffiths, C. E., Baadsgaard, O., Voorhees, J., Hanson, C. & Coopere, K. (1989) Markedly diminished epidermal keratinocyte expression of intercellular adhesion molecule-1 (ICAM-1) in sezary syndrome. JAMA 261, 2217–21.
Nolta, J. A., Sender, L. S., Barranger, J. A. & Khon, D. B. (1990) Expression of human glucocerebrosidase in murine long-term bone marrow cultures after retroviral vector-mediated transfer. Blood 75, 787–97.
Novak, E. K., Hui, S. W. & Swank, R. T. (1984) Platelet storage pool deficiency in mouse pigment mutations associated with seven distinct genetic loci. Blood 63, 536–44.
Novak, E. K., Mcgarry, M. P. & Swank, R. T. (1985) Correction of symptoms of platelet storage pool deficiency in animal models for Chediak-Higashi syndrome and Hermansky-Pudlak syndrome. Blood 66, 1196–201.
Olsen, I., Dean, M. F., Harris, G. & Muir, H. (1981) Direct transfer of a lysosomal enzyme from lymphoid cells to deficient fibroblasts. Nature 291, 244–7.
Olsen, I., Dean, M. F., Muir, H. & Harris, G. (1982) Acquisition of β-glucuronidase activity by deficient fibroblasts during direct contact with lymphoid cells. J. Cell Sci. 55, 211–31.
Olsen, I., Muir, H., Smith, R., Fensom, A. & Watt, D. J. (1983) Direct enzyme transfer from lymphocytes is specific. Nature 306, 75–7.
Olsen, I., Oliver, T., Muir, H., Smith, R. & Partridge, T. (1986) Role of cell adhesion in contact-dependent transfer of a lysosomal enzyme from lymphocytes to fibroblasts. J. Cell Sci. 85, 231–44.
Olsen, I., Abraham, D., Shelton, I., Bou-Gharios, G., Muir, H. & Winchester, B. (1988) Cell contact induces the synthesis of a lysosomal enzyme precursor in lymphocytes and its direct transfer to fibroblasts. Biochim. Biophys. Acta 968, 312–22.
Olsen, I., Bou-Gharios, G. & Abraham, D. (1990) The activation of resting lymphocytes is accompanied by the biogenesis of lysosomal organelles. Eur. J. Immunol. 20, 2161–70.
Pardi, R., Inverardi, L. & Bender, J. R. (1992) Regulatory mechanisms in leukocyte adhesion: flexible receptors for sophisticated travelers. Immunol. Today 13, 224–30.
Partridge, T. A. (1991) Myoblast transfer: A possible therapy for inherited myopathies? Muscle Nerve 14, 197–212.
Peters, P. J., Borst, J., Oorschot, V., Fukuda, M., Krähenbühl, O., Tschopp, J., Slot, J. W. & Geuze, H. J. (1991) Cytotoxic T lymphocyte granules are secretory lysosomes, containing both perforin and granzymes. J. Exp. Med. 173, 1099–109.
Rappeport, J. M., Barranger, J. & Ginns, E. (1986) Bone marrow transplantation in Gaucher disease. In Bone Marrow Transplantation for Treatment of Lysosomal Storage Disease (edited by Krivit, W. & Paul, N.) pp. 101–9. New York: Alan R. Liss.
Reuser, A. J., Kroos, M., Elferink, R. P. J. & Tager, K. M. (1985) Defects in synthesis, phosphorylation, maturation of acid α-glucosidase in glycogenosis type ii. J. Biol. Chem. 260, 8336–41.
Rodman, J. S., Mercer, R. W. & Stahl, P. D. (1990) Endocytosis and trancytosis. Curr. Opin. Cell Biol. 2, 664–72.
Rome, L. H., Garvin, A. J., Allietta, M. M. & Neufeld, E. F. (1979) Two species of lysosomal organelles in cultured human fibroblasts. Cell 17, 143–53.
Rosenberg, S. A., Aebersold, P., Cornetta, K., Kasid, A., Morgan, R. A., Moen, R., Karson, E. M., Lotze, M. T., Yang, J. C. & Topalian, S. L. (1990) Gene transfer into human immunotherapy of patients with advanced melanoma, using tumor-infiltrating lymphocytes modified by retroviral gene transduction. N. Engl. J. Med. 323, 570–8.
Rothberg, K. G., Ying, Y., Kolhouse, J. F., Kamen, B. A. & Anderson, R. G. W. (1990) The glycophospholipid-linked folate receptor internalizes folate without entering the clathrin-coated pit endocytic pathway. J. Cell Biol. 110, 637–49.
Rothberg, K. G., Heuser, J. E., Donzell, W. C., Ying, Y.-S., Glenney, J. R. & Anderson, R. G. W. (1992) Caveolin, a protein component of caveolae membrane coats. Cell 86, 673–82.
Sakiyama, T., Tsuda, M., Owada, M., Kitagawa, T., Miyawaki, S., Shinagawa, T. & Tadokoro, M. (1986) Bone marrow transplantation in Niemann-Pick mice. J. Inher. Metab. Dis. 9, 305–8.
Schuchman, E., Toroyan, T., Haskins, M. & Desnick, R. (1989) Characterization of the defective β-glucuronidase activity in canine mucopolysaccharidosis type VII. Enzyme 42, 174–80.
Scriver, C. R., Beaudet, A. L., Sly, W. S. & Valle, D. (1989) The Metabolic Basis of Inherited Diseases. New York: McGraw Hill.
Singer, K., Le, P., Denning, S. & Whichard, L. (1990) The role of adhesion molecules in epithelial-T-cell interactions in thymus and skin. J. Invest. Dermatol. 94, 85S–91S.
Springer, T. A. (1990) Adhesion receptors of the immune system. Nature 346, 425–34.
Stahl, P. D., Rodman, J. S., Miller, M. J. & Schlesinger, P. H. (1978) Evidence for receptor-mediated binding of glycoprotiens, glycoconjugates, and lysosomal glycosidases by alveolar macrophages. Proc. Natl Acad. Sci. USA 75, 1399–403.
Stahl, P. D., Wileman, T. E. & Sheperd, V. L. (1984) In The Molecular Basis of Lysosomal Storage Disorders (edited by Barranger, J. A. & Brady, R. O.) pp. 209–18. Orlando, FL: Academic Press.
Taylor, M., Farrwo, B. R. H., Stewart, G. J., Healy, P. J. & Tiver, K. (1988) The clinical effects of lysosomal enzyme replacement by bonemarrow transplantation after total lymphoid irradiation on neurologic disease in fucosidase deficient dogs. Trans. Proc. 20, 89–93.
Tran, D., Carpentier, J.-L., Sawano, F., Gorden, P. & Orci, L. (1987) Ligands internalized through coated or noncoated invaginations follow a common intracellular pathway. Proc. Natl Acad. Sci. USA 84, 7957–61.
Tybulewicz, V. L. J., Tremblay, M. L., Lamarca, M. E., Willemsen, R., Stubblefield, B. K., Winfield, S., Zablocka, B., Sidransky, E., Martin, B. M., Huang, S. P., Mintzer, K. A., Westphal, H., Mulligan, R. C. & Ginns, E. L. (1992) Animal model of Gaucher's disease from targeted disruption of the mouse glucocerebrosidase gene. Nature 357, 407–10.
VonFigura, K. & Hasilik, A. (1986) Lysosomal enzymes and their receptors. Annu. Rev. Biochem. 55, 167–93.
Watts, R. W. & Gibbs, D. A. (1986) Lysosomal Storage Diseases: Biochemical and Clinical Aspects. London: Taylor & Francis.
Wileman, T., Harding, C. & Stahl, P. (1985) Receptor-mediated endocytosis. Biochem. J. 232, 1–14.
Wolfe, J. H., Sands, M. S., Barker, J. E., Gwynn, B., Rowe, L. B., Vogler, C. A. & Birkenmeier, E. H. (1992) Reversal of pathology in murine mucopolysaccharidosis type VII by somatic cell gene transfer. Nature 360, 749–53.
Wolff, J. A., Malone, R. W., Williams, P., Chong, W., Acsadi, G., Jani, A. & Feloner, P. L. (1990) Direct gene transfer into mouse muscle in vivo. Science 247, 1465–8.
Yatziv, S., Barfi, G. & Newburg, D. S. (1986) Patients with I-cell disease. J. Lab. Clin. Med. 108, 365–7.
Yeager, A. M. (1990) Bone marrow transplantation in lysosomal storage diseases: a prelude of gene-insertion therapy. Md. Med. J. 39, 337–41.
Yeager, A. M., Brennan, S., Moser, H. W. & Santos, G. W. (1983) Hematopoietic cell transplantation prolongs survival in murine globoid cell leukodystrophy (the Twitcher mouse). Blood 62, 231a.
Yoshie, S. & Ogawa, T. (1983) Occurrence of the myoid cell in the Harderian gland of the Japanese colubrid snake, Rhabdophis tiorinus. Arch. Histol. Japon 46, 131–5.
Yoshikawa, M., Watanabe, M. & Hozumi, N. (1987) Analysis of proteolytic processing during specific antigen presentation. Cell. Immunol. 110, 431–5.
Young, J. D. E. & Cohn, A. (1986) Cell mediated killing: a common mechanism? Cell 46, 641–2.
Young, J. D. E., Liu, C., Pereschini, P. M. & Cohn, Z. (1988) Perforin-dependent and-independent pathways of cytotoxicity mediated by lymphocytes. Immunol. Rev. 103, 161–202.
Author information
Authors and Affiliations
Rights and permissions
About this article
Cite this article
Bou-Gharios, G., Abraham, D. & Olsen, I. Lysosomal storage diseases: mechanisms of enzyme replacement therapy. Histochem J 25, 593–605 (1993). https://doi.org/10.1007/BF00157873
Received:
Revised:
Issue Date:
DOI: https://doi.org/10.1007/BF00157873