Production of MPS VII mouse (Gus™(hE540A.mE536A Sly) doubly tolerant to human and mouse β-glucuronidase

Human Molecular Genetics

Volumn 12, Issue 9, 2003, Pages 961-973

  Tomatsu, Shunji ^a,b   Orii, Koji O ^a,b   Vogler, Carole ^a   Grubb, Jeffrey H ^a   Snella, Elizabeth M ^a   Gutierrez, Monica ^a   Dieter, Tatiana ^a   Holden, Christopher C ^a   Sukegawa, Kazuko ^b   Orii, Tadao ^b   Kondo, Naomi ^b   Sly, William S ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b GIFU UNIVERSITY SCHOOL OF MEDICINE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BETA GLUCURONIDASE; COMPLEMENTARY DNA; MONOMER; TETRAMER;

AGE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AUTOSOMAL RECESSIVE DISORDER; BREEDING METHOD; CONTROLLED STUDY; DNA VECTOR; DOMINANT GENE; DOSE RESPONSE; DRUG EFFICACY; DRUG RESPONSE; DRUG TOLERABILITY; ENZYME ACTIVITY; ENZYME DEFICIENCY; ENZYME REPLACEMENT; ENZYME SYNTHESIS; EXON; FEMALE; GENE EXPRESSION; GENE MUTATION; GENE TARGETING; GENE THERAPY; GERM LINE; HETEROZYGOSITY; HOMOLOGOUS RECOMBINATION; HOMOZYGOSITY; HUMAN; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; INTRON; LONG TERM CARE; LYSOSOME STORAGE DISEASE; MALE; MOUSE; MUCOPOLYSACCHARIDOSIS TYPE 7; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROVOCATION TEST; REVIEW; TISSUE TYPES; TOXICITY TESTING; TRANSGENE; WILD TYPE;

ANIMALS; DISEASE MODELS, ANIMAL; GLUCURONIDASE; HUMANS; MICE; MICE, TRANSGENIC; MUCOPOLYSACCHARIDOSIS VII; MUTATION, MISSENSE;

ANIMALIA; MURINAE;

EID: 0038025993     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/ddg119     Document Type: Review

References (60)

1. Sly, W.S., Quinton, B.A., McAlister, W.H. and Rimoin, D.L. (1973) Beta-glucuronidase deficiency: report of clinical, radiologic, and biochemical features of a new mucopolysaccharidosis. J. Pediatr., 82, 249-257.
2. Neufeld, E.F. and Muenzer, J. (2001) The mucopolysaccharidoses. In Scriver, C.R., Beaudet, A.L., Sly, W.S. and Valle, D. (eds), The Metabolic and Molecular Bases of Inherited Disease. McGraw-Hill, Medical Publishing Division, New York, Vol. 3, pp. 3421-3452.
3. Paigen, K. (1989) Mammalian beta-glucuronidase: genetics, molecular biology, and cell biology. Prog. Nucl. Acid Res. Mol. Biol., 37, 155-205.
4. Tomatsu, S., Sukegawa, K., Ikedo, Y., Fukuda, S., Yamada, Y., Sasaki, T., Okamoto, H., Kuwabara, T. and Orii, T. (1990) Molecular basis of mucopolysaccharidosis type VII: replacement of Ala619 in beta-glucuronidase with Val. Gene, 89, 283-287.
5. Tomatsu, S., Fukuda, S., Sukegawa, K., Ikedo, Y., Yamada, S., Yamada, Y., Sasaki, T., Okamoto, H., Kuwahara, T. and Yamaguchi, S. (1991) Mucopolysaccharidosis type VII: characterization of mutations and molecular heterogeneity. Am. J. Hum. Genet., 48, 89-96.
6. Shipley, J.M., Klinkenberg, M., Wu, B.M., Bachinsky, D.R., Grubb, J.H. and Sly, W.S. (1993) Mutational analysis of a patient with mucopolysaccharidosis type VII, and identification of pseudogenes. Am. J. Hum. Genet., 52, 517-526.
7. Wu, B.M. and Sly, W.S. (1993) Mutational studies in a patient with the hydrops fetalis form of mucopolysaccharidosis type VII. Hum. Mutat., 2, 446-457.
8. Vervoort, R., Lissens, W. and Liebaers, I. (1993) Molecular analysis of a patient with hydrops fetalis caused by beta-glucuronidase deficiency, and evidence for additional pseudogenes. Hum. Mutat., 2, 443-445.
9. Wu, B.M., Tomatsu, S., Fukuda, S., Sukegawa, K., Orii, T. and Sly, W.S. (1994) Overexpression rescues the mutant phenotype of L176F mutation causing beta-glucuronidase deficiency mucopolysaccharidosis in two Mennonite siblings. J. Biol. Chem., 269, 23681-23688.
10. Vervoort, R., Islam, M.R., Sly, W.S., Zabot, M.T., Kleijer, W.J., Chabas, A., Fensom, A., Young, E.P., Liebaers, I. and Lissens, W. (1996) Molecular analysis of patients with beta-glucuronidase deficiency presenting as hydrops fetalis or as early mucopolysaccharidosis VII. Am. J. Hum. Genet., 58, 457-471.
11. Birkenmeier, E.H., Davisson, M.T., Beamer, W.G., Ganschow, R.E., Vogler, C.A., Gwynn, B., Lyford, K.A., Maltais, L.M. and Wawrzyniak, C.J (1989) Murine mucopolysaccharidosis type VII. Characterization of a mouse with beta-glucuronidase deficiency. J. Clin. Invest., 83, 1258-1266
12. Vogler, C., Birkenmeier, E.H., Sly, W.S., Levy, B., Pegors, C., Kyle, J.W. and Beamer, W.G. (1990) A murine model of mucopolysaccharidosis VII. Gross and microscopic findings in beta-glucuronidase-deficient mice. Am. J. Pathol., 136, 207-217.
13. Wolfe, J.H. and Sands, M.S. (1996) Protocols for gene delivery using cells. In Lowenstein, P.R. and Enquist, L.W. (eds), Protocols for Gene Transfer in Neuroscience: Towards Gene Therapy of Neurological Disorders. Wiley, Chichester, pp. 2-45.
14. Birkenmeier, E.H., Barker, J.E., Vogler, C.A., Kyle, J.W., Sly, W.S., Gwynn, B., Levy, B. and Pegors, C. (1991) Increased life span and correction of metabolic defects in murine mucopolysaccharidosis type VII after syngeneic bone marrow transplantation. Blood, 78, 3081-3092.
15. Sands, M.S., Barker, J.E., Vogler, C., Levy, B., Gwynn, B., Galvin, N., Sly, W.S. and Birkenmeier, E. (1993) Treatment of murine mucopolysaccharidosis type VII by syngeneic bone marrow transplantation in neonates. Lab. Invest., 68, 676-686.
16. Bastedo, L., Sands, M., Lambert, D., Pisa, M., Birkenmeier, E. and Chang, P. (1994) Behavioral consequences of bone marrow transplantation in the treatment of murine mucopolysaccharidosis type VII. J. Clin. Invest., 94, 1180-1186.
17. Poorthuis, B.J., Romme, A.E., Willemsen, R. and Wagemaker, G. (1994) Bone marrow transplantation has a significant effect on enzyme levels and storage of glycosaminoglycans in tissues and in isolated hepatocytes of mucopolysaccharidosis type VII mice. Pediatr. Res., 36, 187-193.
18. Sands, M.S., Erway, L.C., Vogler, C., Sly, W.S. and Birkenmeier, E.H. (1995) Syngeneic bone marrow transplantation reduces the hearing loss associated with murine mucopolysaccharidosis type VII. Blood, 86, 2033-2040.
19. Vogler, C., Sands, M., Higgins, A., Levy, B., Grubb, J., Birkenmeier, E.H. and Sly, W.S. (1993) Enzyme replacement with recombinant beta-glucuronidase in the newborn mucopolysaccharidosis type VII mouse. Pediatr. Res., 34, 837-840.
20. Sands, M.S., Vogler, C., Kyle, J.W., Grubb, J.H., Levy, B., Galvin, N., Sly, W.S. and Birkenmeier, E.H. (1994) Enzyme replacement therapy for murine mucopolysaccharidosis type VII. J. Clin. Invest., 93, 2324-2331.
21. Vogler, C., Sands, M.S., Levy, B., Galvin, N., Birkenmeier, E.H. and Sly, W.S. (1996) Enzyme replacement with recombinant beta-glucuronidase in murine mucopolysaccharidosis type VII: impact of therapy during the first six weeks of life on subsequent lysosomal storage, growth, and survival. Pediatr. Res., 39, 1050-1054.
22. O'Connor, L.H., Erway, L.C., Vogler, C.A., Sly, W.S., Nicholes, A., Grubb, J., Holmberg, S.W., Levy, B. and Sands, M.S. (1998) Enzyme replacement therapy for murine mucopolysaccharidosis type VII leads to improvements in behavior and auditory function. J. Clin. Invest., 101, 1394-1400.
23. Vogler, C., Levy, B., Galvin, N.J., Thorpe, C., Sands, M.S., Barker, J.E., Baty, J., Birkenmeier, E.H. and Sly, W.S. (1999) Enzyme replacement in murine mucopolysaccharidosis type VII: neuronal and glial response to beta-glucuronidase requires early initiation of enzyme replacement therapy. Pediatr. Res., 45, 838-844.
24. Soper, B.W., Pung, A.W., Vogler, C.A., Grubb, J.H., Sly, W.S. and Barker, J.E. (1999) Enzyme replacement therapy improves reproductive performance in mucopolysaccharidosis type VII mice but does not prevent postnatal losses. Pediatr. Res., 45, 180-186.
25. Daly, T.M., Lorenz, R.G. and Sands, M.S. (2000) Abnormal immune function in vivo in a murine model of lysosomal storage disease. Pediatr. Res., 47, 757-762.
26. Wolfe, J.H., Sands, M.S., Barker, J.E., Gwynn, B., Rowe, L.B., Vogler, C.A. and Birkenmeier, E.H. (1992) Reversal of pathology in murine mucopolysaccharidosis type VII by somatic cell gene transfer. Nature, 360, 749-753.
27. Moullier, P., Bohl, D., Heard, J.M. and Danos, O. (1993) Correction of lysosomal storage in the liver and spleen of MPS VII mice by implantation of genetically modified skin fibroblasts. Nat. Genet., 4, 154-159.
28. Marechal, V., Naffakh, N., Danos, O. and Heard, J.M. (1993) Disappearance of lysosomal storage in spleen and liver of mucopolysaccharidosis VII mice after transplantation of genetically modified bone marrow cells. Blood, 82, 1358-1365.
29. Taylor, R.M. and Wolfe, J.H. (1997) Decreased lysosomal storage in the adult MPS VII mouse brain in the vicinity of grafts of retroviral vector-corrected fibroblasts secreting high levels of beta-glucuronidase. Nat. Med., 3, 771-774.
30. Gao, C., Sands, M.S., Haskins, M.E. and Ponder, K.P. (2000) Delivery of a retroviral vector expressing human beta-glucuronidase to the liver and spleen decreases lysosomal storage in mucopolysaccharidosis VII mice. Mol. Ther., 2, 233-244.
31. Ohashi, T., Yokoo, T., Iizuka, S., Kobayashi, H., Sly, W.S. and Eto, Y. (2000) Reduction of lysosomal storage in murine mucopolysaccharidosis type VII by transplantation of normal and genetically modified macrophages. Blood, 95, 3631-3633.
32. Brooks, A.I., Stein, C.S., Hughes, S.M., Heth, J., McCray, P.M. Jr, Sauter, S.L., Johnston, J.C., Cory-Slechta, D.A., Federoff, H.J. and Davidson, B.L. (2002) Functional correction of established central nervous system deficits in an animal model of lysosomal storage disease with feline immunodeficiency virus-based vectors. Proc. Natl Acad. Sci. USA, 99, 6216-6221.
33. Xu, L., Mango, R.L., Sands, M.S., Haskins, M.E., Ellinwood, N.M. and Ponder, K.P. (2002) Evaluation of pathological manifestations of disease in mucopolysaccharidosis VII mice after neonatal hepatic gene therapy. Mol. Ther., 6, 745-758.
34. Li, T. and Davidson, B.L. (1995) Phenotype correction in retinal pigment epithelium in murine mucopolysaccharidosis VII by adenovirus-mediated gene transfer. Proc. Natl Acad. Sci. USA, 92, 7700-7704.
35. Ohashi, T., Watabe, K., Uehara, K., Sly, W.S., Vogler, C. and Eto, Y. (1997) Adenovirus-mediated gene transfer and expression of human beta-glucuronidase gene in the liver, spleen, and central nervous system in mucopolysaccharidosis type VII mice. Proc. Natl Acad. Sci. USA, 94, 1287-1292.
36. Ghodsi, A., Stein, C., Derksen, T., Yang, G., Anderson, R.D. and Davidson, B.L. (1998) Extensive beta-glucuronidase activity in murine central nervous system after adenovirus-mediated gene transfer to brain. Hum. Gene Ther., 9, 2331-2340.
37. Ghodsi, A., Stein, C., Derksen, T., Martins, I., Anderson, R.D. and Davidson, B.L. (1999) Systemic hyperosmolality improves beta-glucuronidase distribution and pathology in murine MPS VII brain following intraventricular gene transfer. Exp. Neurol., 160, 109-116.
38. Kosuga, M., Takahashi, S., Sasaki, K., Li, X.K., Fujino, M., Hamada, H., Suzuki, S., Yamada, M., Matsuo, N. and Okuyama, T. (2000) Adenovirus-mediated gene therapy for mucopolysaccharidosis VII: involvement of cross-correction in wide-spread distribution of the gene products and long-term effects of CTLA-4Ig coexpression. Mol. Ther., 1, 406-413.
39. Watson, G.L., Sayles, J.N., Chen, C., Elliger, S.S., Elliger, C.A., Raju, N.R., Kurtzman, G.J. and Podsakoff, G.M. (1998) Treatment of lysosomal storage disease in MPS VII mice using a recombinant adeno-associated virus. Gene Ther., 5, 1642-1649.
40. Daly, T.M., Vogler, C., Levy, B., Haskins, M.E. and Sands, M.S. (1999) Neonatal gene transfer leads to widespread correction of pathology in a murine model of lysosomal storage disease. Proc. Natl Acad. Sci. USA, 96, 2296-2300.
41. Daly, T.M., Okuyama, T., Vogler, C., Haskins, M.E., Muzyczka, N. and Sands, M.S. (1999) Neonatal intramuscular injection with recombinant adeno-associated virus results in prolonged beta-glucuronidase expression in situ and correction of liver pathology in mucopolysaccharidosis type VII mice. Hum. Gene Ther., 10, 85-94.
42. Skorupa, A.F., Fisher, K.J., Wilson, J.M., Parente, M.K. and Wolfe, J.H. (1999) Sustained production of beta-glucuronidase from localized sites after AAV vector gene transfer results in widespread distribution of enzyme and reversal of lysosomal storage lesions in a large volume of brain in mucopolysaccharidosis VII mice. Exp. Neurol., 160, 17-27.
43. Sferra, T.J., Qu, G., McNeely, D., Rennard, R., Clark, K.R., Lo, W.D. and Johnson, P.R. (2000) Recombinant adeno-associated virus-mediated correction of lysosomal storage within the central nervous system of the adult mucopolysaccharidosis type VII mouse. Hum. Gene Ther., 11, 507-519.
44. Bosch, A., Perret, E., Desmaris, N. and Heard, J.M. (2000) Long-term and significant correction of brain lesions in adult mucopolysaccharidosis type VII mice using recombinant AAV vectors. Mol. Ther., 1, 63-70.
45. Kakkis, E.D., McEntee, M.F., Schmidtchen, A., Neufeld, E.F., Ward, D.A., Gompf, R.E., Kania, S., Bedolla, C., Chien, S.L. and Shull, R.M. (1996) Long-term and high-dose trials of enzyme replacement therapy in the canine model of mucopolysaccharidosis I. Biochem. Mol. Med., 58, 156-167.
46. Shull, R.M., Lu, X., McEntee, M.F., Bright, R.M., Pepper, K.A. and Kohn, D.B. (1996) Myoblast gene therapy in canine mucopolysaccharidosis. I: abrogation by an immune response to alpha-L-iduronidase. Hum. Gene Ther., 7, 1595-1603.
47. Wong, A.W., He, S., Grubb, J.H., Sly, W.S. and Withers, S.G. (1998) Identification of Glu-540 as the catalytic nucleophile of human beta-glucuronidase using electrospray mass spectrometry J. Biol. Chem., 273, 34057-34062.
48. Islam, M.R., Tomatsu, S., Shah, G.N., Grubb, J.H., Jain, S. and Sly, W.S. (1999) Active site residues of human beta-glucuronidase. Evidence for Glu(540) as the nucleophile and Glu(451) as the acid-base residue. J. Biol. Chem., 274, 23451-23455.
49. Sly, W.S., Vogler, C., Grubb, J.H., Zhou, M., Jiang, J., Zhou, X.Y., Tomatsu, S., Bi, Y. and Snella, E.M. (2001) Active site mutant transgene confers tolerance to human beta-glucuronidase without affecting the phenotype of MPS VII mice. Proc. Natl Acad. Sci. USA, 98, 2205-2210.
50. Sands, M.S., Vogler, C., Torrey, A., Levy, B., Gwynn, B., Grubb, J., Sly, W.S. and Birkenmeier, E.H. (1997) Murine mucopolysaccharidosis type VII: long term therapeutic effects of enzyme replacement and enzyme replacement followed by bone marrow transplantation. J. Clin. Invest., 99, 1596-1605.
51. Crawley, A.C., Niedzielski, K.H., Isaac, E.L., Davey, R.C., Byers, S. and Hopwood, J.J. (1997) Enzyme replacement therapy from birth in a feline model of mucopolysaccharidosis type VI. J. Clin. Invest., 99, 651-662.
52. Kakkis, E.D., Schuchman, E., He, X., Wan, Q., Kania, S., Wiemelt, S., Hasson, C.W., O'Malley, T., Weil, M.A., Aguirre, G.A., Brown, D.E. and Haskins, M.E. (2001) Enzyme replacement therapy in feline mucopolysaccharidosis I. Mol. Genet. Metab, 72, 199-208.
53. Tripathy, S.K., Black, H.B., Goldwasser, E. and Leiden, J.M. (1996) Immune responses to transgene-encoded proteins limit the stability of gene expression after injection of replication-defective adenovirus vectors. Nat. Med., 2, 545-550.
54. Li, H.H., Yu, W.H., Rozengurt, N., Zhao, H.Z., Lyons, K.M., Anagnostaras, S., Fanselow, M.S., Suzuki, K., Vanier, M.T. and Neufeld, E.F. (1999) Mouse model of Sanfilippo syndrome type B produced by targeted disruption of the gene encoding alpha-N-acetylglucosaminidase. Proc. Natl Acad. Sci. USA, 96, 14505-14510.
55. Jain, S., Drendel, W.B., Chen, Z.W., Mathews, F.S., Sly, W.S. and Grubb, J.H. (1996) Structure of human beta-glucuronidase reveals candidate lysosomal targeting and active-site motifs. Nat. Struct. Biol., 3, 375-381.
56. Wagner, T.E., Hoppe, P.C., Jollick, J.D., Scholl, D.R., Hodinka, R.L. and Gault, J.B. (1981) Microinjection of a rabbit beta-globin gene into zygotes and its subsequent expression in adult mice and their offspring. Proc. Nad Acad. Sci. USA, 78, 6376-6380.
57. Glaser, J.H. and Sly, W.S. (1973) Beta-glucuronidase deficiency mucopolysaccharidosis: methods for enzymatic diagnosis. J. Lab. Clin. Med., 82, 969-977.
58. Peterson, G.L. (1979) Review of the Folin phenol protein quantitation method of Lowry, Rosebrough, Farr and Randall. Anal. Biochem., 100, 201-220.
59. Bjornsson, S. (1993) Simultaneous preparation and quantitation of proteoglycans by precipitation with alcian blue. Anal. Biochem., 210, 282-291.
60. Whitley, C.B., Ridnour, M.D., Draper, K.A., Dutton, C.M. and Neglia, J.P. (1989) Diagnostic test for mucopolysaccharidosis. I. Direct method for quantifying excessive urinary glycosaminoglycan excretion. Clin. Chem., 35, 374-379.