Pharmacological chaperone therapy for Fabry disease

Proceedings of the Japan Academy Series B: Physical and Biological Sciences

Volumn 88, Issue 1, 2012, Pages 18-30

  Ishii, Satoshi ^a,b  

^a OITA UNIVERSITY   (Japan)

^b Biochemical Laboratory   (Japan)

Author keywords

galactosidase A; Fabry disease; Pharmacological chaperone; Therapy

Indexed keywords

1 DEOXYNOJIRIMYCIN; 1-DEOXYGALACTONOJIRIMYCIN; ALPHA GALACTOSIDASE; DRUG DERIVATIVE; MIGALASTAT; MUTANT PROTEIN;

ANIMAL; CLINICAL TRIAL (TOPIC); DISEASE MODEL; DRUG EFFECT; ENZYMOLOGY; FABRY DISEASE; FEMALE; GENETICS; HUMAN; IMMUNOHISTOCHEMISTRY; MALE; METABOLISM; MOUSE; MUTATION; PATHOLOGY; PROTEIN FOLDING; REVIEW; ULTRASTRUCTURE;

1-DEOXYNOJIRIMYCIN; ALPHA-GALACTOSIDASE; ANIMALS; CLINICAL TRIALS AS TOPIC; DISEASE MODELS, ANIMAL; FABRY DISEASE; FEMALE; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; MICE; MUTANT PROTEINS; MUTATION; PROTEIN FOLDING;

MAMMALIA; MUS MUSCULUS;

EID: 84856411368     PISSN: 03862208     EISSN: 13492896     Source Type: Journal    
DOI: 10.2183/pjab.88.18     Document Type: Review

References (68)

1. Brady, O.R., Gal, A.E., Bradley, R.M., Martensson, E., Warshaw, A.L. and Laster, L. (1967) Enzymatic defect in Fabry's disease: Ceramidetrihexosidase deficiency. N. Engl. J. Med. 276, 1163-1167.
2. Askari, H., Kaneski, C.R., Semino-Mora, C., Desai, P., Ang, A., Kleiner, D.E., Perlee, L.T., Quezado, M., Spollen, L.E., Wustman, B.A. and Schiffmann, R. (2007) Cellular and tissue localization of globotriaosylceramide in Fabry disease. Virchows Arch. 451, 823-834.
3. Pabico, R.C., Atancio, B.C., McKenna, B.A., Pamukcoglu, T. and Yodaiken, R. (1973) Renal pathologic lesions and functional alterations in a man with Fabry's disease. Am. J. Med. 55, 415-425.
4. Desnick, R.J., Ioannou, Y.A. and Eng, C.M. (2001) Fabry disease. In The Metabolic and Molecular Bases of Inherited Disease (eds. Scriver, C.R., Beaudet, A.L., Sly, W.S. and Valle, D.). McGraw-Hill, New York, pp. 3733-3774.
5. von Scheidt, W., Eng, C.M., Fitzmaurice, T.F., Erdmann, E., Hubner, G., Olsen, E.G., Christomanou, H., Kandolf, R., Bishop, D.F. and Desnick, R.J. (1991) An atypical variant of Fabry's disease with manifestations confined to the myocardium. N. Engl. J. Med. 324, 395-399.
6. Nakao, S., Takenaka, T., Maeda, M., Kodama, C., Tanaka, A., Tahara, M., Yoshida, A., Kuriyama, M., Hayashibe, H., Sakuraba, H. and Tanaka, H. (1995) An atypical variant of Fabry's disease in men with left ventricular hypertrophy. N. Engl. J. Med. 333, 288-293.
7. Nakao, S., Kodama, C., Takenaka, T., Tanaka, A., Yasumoto, Y., Yoshida, A., Kanzaki, T., Enriquez, A.L.D., Eng, C.M., Tanaka, H., Tei, C. and Desnick, R.J. (2003) Fabry disease: Detection of undiagnosed hemodialysis patients and identification of a "renal variant" phenotype. Kidney Int. 64, 801-807.
8. Bekri, S., Enica, A., Ghafari, T., Plaza, G., Champenois, I., Choukroun, G., Unwin, R. and Jaeger, P. (2005) Fabry disease in patients with end-stage renal failure: the potential benefits of screening. Nephron Clin. Pract. 101, c33-c38.
9. Eng, C.M., Guffon, N., Wilcox, W.R., Germain, D.P., Lee, P., Waldek, S., Caplan, L., Linthorst, G.E. and Desnick, R.J.; International Collaborative Fabry Disease Study Group (2001) Safety and efficacy of recombinant human α-galactosidase A replacement therapy in Fabry's disease. N. Engl. J. Med. 345, 9-16.
10. Schiffmann, R.S., Kopp, J.B., Austin, H.A., Sabnis, S., Moore, D.F., Wiebel, T., Balow, J.E. and Brady, R.O. (2001) Enzyme replacement therapy in Fabry disease. JAMA 285, 2743-2749.
11. Schiffmann, R., Ries, M., Timmons, M., Flaherty, J.T. and Brady, R.O. (2006) Long-term therapy with agalsidase alfa for Fabry disease: safety and effects on renal function in a home infusion setting. Nephrol. Dial. Transplant. 21, 345-354.
12. Schiffmann, R., Askari, H., Timmons, M., Robinson, C., Benko, W., Brady, R.O. and Ries, M. (2007) Weekly enzyme replacement therapy may slow decline of renal function in patients with Fabry disease who are on long-term biweekly dosing. J. Am. Soc. Nephrol. 18, 1576-1583.
13. Hughes, D.A., Elliott, P.M., Shah, J., Zuckerman, J., Coghlan, G., Brookes, J. and Mehta, A.B. (2008) Effects of enzyme replacement therapy on the cardiomyopathy of Anderson-Fabry disease: a randomised, double-blind, placebo-controlled clinical trial of agalsidase alfa. Heart 94, 153-158.
14. Kampmann, C., Linhart, A., Devereux, R.B. and Schiffmann, R. (2009) Effect of agalsidase alfa replacement therapy on Fabry disease-related hypertrophic cardiomyopathy: a 12- to 36-month, retrospective, blinded echocardiographic pooled analysis. Clin. Ther. 31, 1966-1976.
15. Mehta, A., Beck, M., Elliott, P., Giugliani, R., Linhart, A., Sunder-Plassmann, G., Schiffmann, R., Barbey, F., Ries, M. and Clarke, J.T. Fabry Outcome Survey investigators (2009) Enzyme replacement therapy with agalsidase alfa in patients with Fabry's disease: an analysis of registry data. Lancet 374, 1986-1996.
16. Beutler, E. (2006) Lysosomal storage diseases: natural history and ethical and economic aspects. Mol. Genet. Metab. 88, 208-215.
17. Fan, J.-Q., Ishii, S., Asano, N. and Suzuki, Y. (1999) Accelerated transport and maturation of lysosomal α-galactosidase A in Fabry lymphoblasts by an enzyme inhibitor. Nat. Med. 5, 112-115.
18. Bishop, D.F., Calhoun, D.H., Bernstein, H.S., Hantzopoulos, P., Quinn, M. and Desnick, R.J. (1986) Human α-galactosidase A: Nucleotide sequence of a cDNA clone encoding the mature enzyme. Proc. Natl. Acad. Sci. U.S.A. 83, 4859-4863.
19. Ishii, S., Sakuraba, H. and Suzuki, Y. (1992) Point mutations in the upstream region of the α-galactosidase A gene exon 6 in an atypical variant of Fabry disease. Hum. Genet. 89, 29-32.
20. Ishii, S., Kase, R., Sakuraba, H., Fujita, S., Sugimoto, M., Tomita, K., Semba, T. and Suzuki, Y. (1994) Human α-galactosidase gene expression: Significance of two peptide regions encoded by exons 1-2 and 6. Biochim. Biophys. Acta 1204, 265-270.
21. Ishii, S., Kase, R., Sakuraba, H. and Suzuki, Y. (1993) Characterization of a mutant α-galactosidase gene product for the late-onset cardiac form of Fabry disease. Biochem. Biophys. Res. Commun. 197, 1585-1589.
22. Kase, R., Bierfreund, U., Klein, A., Kolter, T., Utsumi, K., Itoh, K., Sandhoff, K. and Sakuraba, H. (2000) Characterization of two α-galactosidase mutants (Q279E and R301Q) found in an atypical variant of Fabry disease. Biochim. Biophys. Acta 1501, 227-235.
23. Asano, N., Kato, A., Oseki, K., Kizu, H. and Matsui, K. (1995) Calystegins of Physalis alkekengi var. francheti (Solanaceae). Structure determination and their glycosidase inhibitory activities. Eur. J. Biochem. 229, 369-376.
24. Asano, N., Kato, A., Miyauchi, M., Kizu, H., Tomimori, T., Matsui, K., Nash, R.J. and Molyneux, R.J. (1997) Specific α-galactosidase inhibitors, N-methylcalystegines-structure/activity relationships of calystegines from Lycium chinense. Eur. J. Biochem. 248, 296-303.
25. Asano, N., Kato, A., Matsui, K., Watson, A.A., Nash, R.J., Molyneux, R.J., Hackett, L., Topping, J. and Winchester, B. (1997) The effects of calystegines isolated from edible fruits and vegetables on mammalian liver glycosidases. Glycobiology 7, 1085-1088.
26. Asano, N., Ishii, S., Kizu, H., Ikeda, K., Yasuda, K., Kato, A., Martin, O.R. and Fan, J.-Q. (2000) In vitro inhibition and intracellular enhancement of lysosomal α-galactosidase A activity in Fabry lymphoblasts by 1-deoxygalactonojirimycin and its derivatives. Eur. J. Biochem. 267, 4179-4186.
27. Hurtley, S.M. and Helenius, A. (1989) Protein oligomerization in the endoplasmic reticulum. Annu. Rev. Cell Biol. 5, 277-307.
28. Klausner, R.D. and Sitia, R. (1990) Protein degradation in the endoplasmic reticulum. Cell 62, 611-614.
29. Ellgaard, L. and Helenius, A. (2003) Quality control in the endoplasmic reticulum. Nat. Rev. Mol. Cell Biol. 4, 181-191.
30. Kuznetsov, G. and Nigam, S.K. (1998) Folding of secretory and membrane proteins. N. Engl. J. Med. 339, 1688-1695.
31. Thomas, P.J., Qu, B.H. and Pedersen, P.L. (1995) Defective protein folding as a basis of human disease. Trends Biochem. Sci. 20, 456-459.
32. Cohen, F.E. and Kelly, J.W. (2003) Therapeutic approaches to protein-misfolding diseases. Nature 426, 905-909.
33. Garman, S.C. and Garboczi, D.N. (2004) The molecular defect leading to Fabry disease: Structure of human α-galactosidase. J. Mol. Biol. 337, 319-335.
34. Matsuzawa, F., Aikawa, S., Doi, H., Okumiya, T. and Sakuraba, H. (2005) Fabry disease: correlation between structural changes in α-galactosidase, and clinical and biochemical phenotypes. Hum. Genet. 117, 317-328.
35. Ishii, S., Yoshioka, H., Mannen, K., Kulkarni, A.B. and Fan, J.-Q. (2004) Transgenic mouse expressing human mutant α-galactosidase A in an endogenous enzyme deficient background: a biochemical animal model for studying active-site specific chaperone therapy for Fabry disease. Biochim. Biophys. Acta 1690, 250-257.
36. Lemansky, P., Bishop, D.F., Desnick, R.J., Hasilik, A. and von Figura, K. (1987) Synthesis and processing of α-galactosidase A in human fibroblasts. Evidence for different mutations in Fabry disease. J. Biol. Chem. 262, 2062-2065.
37. Ishii, S., Chang, H.-H., Kawasaki, K., Yasuda, K., Wu, H.-L., Garman, S.C. and Fan, J.-Q. (2007) Mutant α-galactosidase A enzymes identified in Fabry patients with residual enzyme activity: biochemical characterization and restoration of normal intracellular processing by 1-deoxygalactonojirimycin. Biochem. J. 406, 285-295.
38. Hamanaka, R., Shinohara, T., Yano, S., Nakamura, M., Yasuda, A., Yokoyama, S., Fan, J.-Q., Kawasaki, K., Watanabe, M. and Ishii, S. (2008) Rescue of mutant α-galactosidase A in the endoplasmic reticulum by 1-deoxygalactonojirimycin leads to trafficking to lysosomes. Biochim. Biophys. Acta 1782, 408-413.
39. Bishop, D.F., Kornreich, R. and Desnick, R.J. (1988) Structural organization of the human α-galactosidase A gene: further evidence for the absence of a 3' untranslated region. Proc. Natl. Acad. Sci. U.S.A. 85, 3903-3907.
40. Yam, G.H., Zuber, C. and Roth, J. (2005) A synthetic chaperone corrects the trafficking defect and disease phenotype in a protein misfolding disorder. FASEB J. 19, 12-18.
41. Fan, J.-Q. and Ishii, S. (2007) Active-site-specific chaperone therapy for Fabry disease: Yin and Yang of enzyme inhibitors. FEBS J. 274, 4962-4971.
42. Yam, G.H., Bosshard, N., Zuber, C., Steinmann, B. and Roth, J. (2006) Pharmacological chaperone corrects lysosomal storage in Fabry disease caused by trafficking-incompetent variants. Am. J. Physiol. Cell Physiol. 290, C1076-C1082.
43. Shiozuka, C., Taguchi, A., Matsuda, J., Noguchi, Y., Kunieda, T., Uchio-Yamada, K., Yoshioka, H., Hamanaka, R., Yano, S., Yokoyama, S., Mannen, K., Kulkarni, A.B., Furukawa, K. and Ishii, S. (2011) Increased globotriaosylceramide levels in a transgenic mouse expressing human alpha1,4-galactosyltransferase and a mouse model for treating Fabry disease. J. Biochem. 149, 161-170.
44. Shimmoto, M., Kase, R., Itoh, K., Utsumi, K., Ishii, S., Taya, C., Yonekawa, H. and Sakuraba, H. (1997) Generation and characterization of transgenic mice expressing a human mutant α-galactosidase with an R301Q substitution causing a variant form of Fabry disease. FEBS Lett. 417, 89-91.
45. Ohshima, T., Murray, G.J., Swaim, W.D., Longenecker, G., Quirk, J.M., Cardarelli, C.O., Sugimoto, Y., Pastan, I., Gottesman, M.M., Brady, R.O. and Kulkarni, A.B. (1997) α-galactosidase A deficient mice: A model of Fabry disease. Proc. Natl. Acad. Sci. U.S.A. 94, 2540-2544.
46. Ishii, S., Chang, H.-H., Yoshioka, H., Shimada, T., Mannen, K., Higuchi, Y., Taguchi, A. and Fan, J.-Q. (2009) Preclinical efficacy and safety of 1-deoxygalactonojirimycin in mice for Fabry disease. J. Pharmacol. Exp. Ther. 328, 723-731.
47. Eng, C.M., Banikazemi, M., Gordon, R.E., Goldman, M., Phelps, R., Kim, L., Gass, A., Winston, J., Dikman, S., Fallon, J.T., Brodie, S., Stacy, C.B., Mehta, D., Parsons, R., Norton, K., O'Callaghan, M. and Desnick, R.J. (2001) A phase 1/2 clinical trial of enzyme replacement in Fabry disease: Pharmacokinetic, substrate clearance and safety studies. Am. J. Hum. Genet. 68, 711-722.
48. Khanna, R., Soska, R., Lun, Y., Feng, J., Franscella, M., Young, B., Brignol, N., Pellegrino, L., Sitaraman, S., Desnick, R.J., Benjamin, E.R., Lockhart, D.J. and Valenzano, K.J. (2010) The pharmacological chaperone 1-deoxygalactonojirimycin reduces tissue globotriaosylceramide levels in a mouse model of Fabry disease. Mol. Ther. 18, 23-33.
49. Frustaci, A., Chimenti, C., Ricci, R., Natale, L., Russo, M.A., Pieroni, M., Eng, C.M. and Desnick, R.J. (2001) Improvement in cardiac function in the cardiac variant of Fabry's disease with galactoseinfusion therapy. N. Engl. J. Med. 345, 25-32.
50. Porto, C., Cardone, M., Fontana, F., Rossi, B., Tuzzi, M.R., Tarallo, A., Barone, M.V., Andria, G. and Parenti, G. (2009) The pharmacological chaperone N-butyldeoxynojirimycin enhances enzyme replacement therapy in Pompe disease fibroblasts. Mol. Ther. 17, 964-971.
51. Sawkar, A.R., Cheng, W.C., Beutler, E., Wong, C.H., Balch, W.E. and Kelly, J.W. (2002) Chemical chaperones increase the cellular activity of N370S ß-glucosidase: a therapeutic strategy for Gaucher disease. Proc. Natl. Acad. Sci. U.S.A. 99, 15428-15433.
52. Cheng, H.H., Asano, N., Ishii, S., Ichikawa, Y. and Fan, J.-Q. (2006) Hydrophilic iminosugar activesite-specific chaperones increase residual glucocerebrosidase activity in fibroblasts from Gaucher patients. FEBS J. 273, 4082-4092.
53. Matsuda, J., Suzuki, O., Oshima, A., Yamamoto, Y., Noguchi, A., Takimoto, K., Itoh, M., Matsuzaki, Y., Yasuda, Y., Ogawa, S., Sakata, Y., Nanba, E., Higaki, K., Ogawa, Y., Tominaga, L., Ohno, K., Iwasaki, H., Watanabe, H., Brady, R.O. and Suzuki, Y. (2003) Chemical chaperone therapy for brain pathology in G(M1)-gangliosidosis. Proc. Natl. Acad. Sci. U.S.A. 100, 15912-15917.
54. Tropak, M.B., Reid, S.P., Guiral, M., Withers, S.G. and Mahuran, D. (2004) Pharmacological enhancement of ß-hexosaminidase activity in fibroblasts from adult Tay-Sachs and Sandhoff patients. J. Biol. Chem. 279, 13478-13487.
55. Okumiya, T., Kroos, M.A., Vliet, L.V., Takeuchi, H., Van der Ploeg, A.T. and Reuser, A.J. (2007) Chemical chaperones improve transport and enhance stability of mutant,-glucosidases in glycogen storage disease type II. Mol. Genet. Metab. 90, 49-57.
56. Bonapace, G., Waheed, A., Shah, G.N. and Sly, W.S. (2004) Chemical chaperones protect from effects of apoptosis-inducing mutation in carbonic anhydrase IV identified in retinitis pigmentosa 17. Proc. Natl. Acad. Sci. U.S.A. 101, 12300-12305.
57. Bernier, V., Morello, J.P., Zarruk, A., Debrand, N., Salahpour, A., Lonergan, M., Arthus, M.F., Laperrière, A., Brouard, R., Bouvier, M. and Bichet, D.G. (2006) Pharmacologic chaperones as a potential treatment for X-linked nephrogenic diabetes insipidus. J. Am. Soc. Nephrol. 17, 232-243.
58. Pey, A.L., Ying, M., Cremades, N., Velazquez-Campoy, A., Scherer, T., Thöny, B., Sancho, J. and Martinez, A. (2008) Identification of pharmacological chaperones as potential therapeutic agents to treat phenylketonuria. J. Clin. Invest. 118, 2858-2867.
59. Wang, X., Koulov, A.V., Kellner, W.A., Riordan, J.R. and Balch, W.E. (2008) Chemical and biological folding contribute to temperature-sensitive δF508 CFTR trafficking. Traffic 9, 1878-1893.
60. Benjamin, E.R., Flanagan, J.J., Schilling, A., Chang, H.H., Agarwal, L., Katz, E., Wu, X., Pine, C., Wustman, B., Desnick, R.J., Lockhart, D.J. and Valenzano, K.J. (2009) The pharmacological chaperone 1-deoxygalactonojirimycin increases alphagalactosidase A levels in Fabry patient cell lines. J. Inherit. Metab. Dis. 32, 424-440.
61. Wu, X., Katz, E., Valle, M.C., Mascioli, K., Flanagan, J.J., Castelli, J.P., Schiffmann, R., Boudes, P., Lockhart, D.J., Valenzano, K.J. and Benjamin, E.R. (2011) A pharmacogenetic approach to identify mutant forms of α-galactosidase A that respond to a pharmacological chaperone for Fabry disease. Hum. Mutat. 32, 965-977.
62. Shin, S.H., Kluepfel-Stahl, S., Cooney, A.M., Kaneski, C.R., Quirk, J.M., Schiffmann, R., Brady, R.O. and Murray, G.J. (2008) Prediction of response of mutated α-galactosidase A to a pharmacological chaperone. Pharmacogenet. Genomics 18, 773-780.
63. Shimotori, M., Maruyama, H., Nakamura, G., Suyama, T., Sakamoto, F., Itoh, M., Miyabayashi, S., Ohnishi, T., Sakai, N., Wataya-Kaneda, M., Kubota, M., Takahashi, T., Mori, T., Tamura, K., Kageyama, S., Shio, N., Maeba, T., Yahagi, H., Tanaka, M., Oka, M., Sugiyama, H., Sugawara, T., Mori, N., Tsukamoto, H., Tamagaki, K., Tanda, S., Suzuki, Y., Shinonaga, C., Miyazaki, J., Ishii, S. and Gejyo, F. (2008) Novel mutations of the GLA gene in Japanese patients with Fabry disease and their functional characterization by active site specific chaperone. Hum. Mutat. 29, 331.
64. Park, J.Y., Kim, G.H., Kim, S.S., Ko, J.M., Lee, J.J. and Yoo, H.W. (2009) Effects of a chemical chaperone on genetic mutations in α-galactosidase A in Korean patients with Fabry disease. Exp. Mol. Med. 41, 1-7.
65. Spada, M., Pagliardini, S., Yasuda, M., Tukel, T., Thiagarajan, G., Sakuraba, H., Ponzone, A. and Desnick, R.J. (2006) High incidence of later-onset Fabry disease revealed by newborn screening. Am. J. Hum. Genet. 79, 31-40.
66. Ferri, L., Guido, C., La Marca, G., Malvagia, S., Cavicchi, C., Fiumara, A., Barone, R., Parini, R., Antuzzi, D., Feliciani, C., Zampetti, A., Manna, R., Giglio, S., Della Valle, C., Wu, X., Valenzano, K., Benjamin, E., Donati, M., Guerrini, R., Genuardi, M. and Morrone, A. (2011) Fabry disease: polymorphic haplotypes and a novel missense mutation in the GLA gene. Clin. Genet. doi: 10.1111/j.1399-0004.2011.01689.x.
67. Shin, S.H., Murray, G.J., Kluepfel-Stahl, S., Cooney, A.M., Quirk, J.M., Schiffmann, R., Brady, R.O. and Kaneski, C.R. (2007) Screening for pharmacological chaperones in Fabry disease. Biochem. Biophys. Res. Commun. 359, 168-173.
68. Filoni, C., Caciotti, A., Carraresi, L., Cavicchi, C., Parini, R., Antuzzi, D., Zampetti, A., Feriozzi, S., Poisetti, P., Garman, S.C., Guerrini, R., Zammarchi, E., Donati, M.A. and Morrone, A. (2010) Functional studies of new GLA gene mutations leading to conformational Fabry disease. Biochim. Biophys. Acta 1802, 247-252.