GM1 gangliosidosis: Review of clinical, molecular, and therapeutic aspects

Molecular Genetics and Metabolism

Volumn 94, Issue 4, 2008, Pages 391-396

  Brunetti Pierri, Nicola ^a   Scaglia, Fernando ^a,b  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b TEXAS CHILDREN S HOSPITAL   (United States)

Author keywords

galactosidase; GLB1; GM1 gangliosidosis; Lysosomal storage disorders

Indexed keywords

ADENOVIRUS VECTOR; BETA GALACTOSIDASE; CHAPERONE; IMINOSUGAR; N OCTYL 4 EPI BETA VALIENAMINE; PARVOVIRUS VECTOR;

ALLOGENIC BONE MARROW TRANSPLANTATION; CLINICAL FEATURE; DRUG ACTIVITY; DRUG DELIVERY SYSTEM; DRUG EFFICACY; ENZYME ACTIVITY; GENE THERAPY; GLOBOID CELL LEUKODYSTROPHY; GM1 GANGLIOSIDOSIS; HUMAN; MUTATIONAL ANALYSIS; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; ADOLESCENT; ADULT; AMINO ACID SEQUENCE; ANIMAL; CHEMISTRY; CHILD; DISEASE MODEL; FEMALE; GENETICS; INFANT; MALE; METABOLISM; MUTATION; PATHOLOGY; PRESCHOOL CHILD;

ANIMALIA;

ADOLESCENT; ADULT; AMINO ACID SEQUENCE; ANIMALS; BETA-GALACTOSIDASE; CHILD; CHILD, PRESCHOOL; DISEASE MODELS, ANIMAL; FEMALE; GANGLIOSIDOSIS, GM1; HUMANS; INFANT; MALE; MUTATION;

EID: 46749113388     PISSN: 10967192     EISSN: 10967206     Source Type: Journal    
DOI: 10.1016/j.ymgme.2008.04.012     Document Type: Review

References (74)

1. Okada S., and O'Brien J.S. Generalized gangliosidosis: beta-galactosidase deficiency. Science 160 (1968) 1002-1004
2. Sinigerska I., Chandler D., Vaghjiani V., Hassanova I., Gooding R., Morrone A., Kremensky I., and Kalaydjieva L. Founder mutation causing infantile GM1-gangliosidosis in the Gypsy population. Mol. Genet. Metab. 88 (2006) 93-95
3. Coelho J.C., Wajner M., Burin M.G., Vargas C.R., and Giugliani R. Selective screening of 10,000 high-risk Brazilian patients for the detection of inborn errors of metabolism. Eur. J. Pediatr. 156 (1997) 650-654
4. Severini M.H., Silva C.D., Sopelsa A., Coelho J.C., and Giugliani R. High frequency of type 1 GM1 gangliosidosis in southern Brazil. Clin. Genet. 56 (1999) 168-169
5. Santamaria R., Chabas A., Coll M.J., Miranda C.S., Vilageliu L., and Grinberg D. Twenty-one novel mutations in the GLB1 gene identified in a large group of GM1-gangliosidosis and Morquio B patients: possible common origin for the prevalent p.R59H mutation among gypsies. Hum. Mutat. 27 (2006) 1060
6. Lenicker H.M., Vassallo Agius P., Young E.P., and Attard Montalto S.P. Infantile generalized GM1 gangliosidosis: high incidence in the Maltese Islands. J. Inherit. Metab. Dis. 20 (1997) 723-724
7. Georgiou T., Stylianidou G., Anastasiadou V., Caciotti A., Campos Y., Zammarchi E., Morrone A., D'Azzo A., and Drousiotou A. The Arg482His mutation in the beta-galactosidase gene is responsible for a high frequency of GM1 gangliosidosis carriers in a Cypriot village. Genet. Test. 9 (2005) 126-132
8. 1-gangliosidosis and Morquio B disease. The Metabolic and Molecular Basis of Inherited Disease (2001), McGraw-Hill, New York
9. Suzuki Y., Nakamura N., and Fukuoka K. GM1-gangliosidosis: accumulation of ganglioside GM1 in cultured skin fibroblasts and correlation with clinical types. Hum. Genet. 43 (1978) 127-131
10. Wenger D.A., Tarby T.J., and Wharton C. Macular cherry-red spots and myoclonus with dementia: coexistent neuraminidase and beta-galactosidase deficiencies. Biochem. Biophys. Res. Commun. 82 (1978) 589-595
11. G. Andria, G. Pontarelli, W.S. Sly, W.E. Dodson, in: G. Tettamanti, P. Durand, S.D. DiDonato (eds.), Infantile neuraminidase and β-galactosidase deficiencies (galactosialidosis) with mild clinical courses (Sialidases and Sialidoses), Edi Ermes, Milan, Italy, 1981, pp. 379.
12. Galjart N.J., Gillemans N., Harris A., van der Horst G.T., Verheijen F.W., Galjaard H., and d'Azzo A. Expression of cDNA encoding the human "protective protein" associated with lysosomal beta-galactosidase and neuraminidase: homology to yeast proteases. Cell 54 (1988) 755-764
13. D'Azzo A., Hoogeveen A., Reuser A.J., Robinson D., and Galjaard H. Molecular defect in combined beta-galactosidase and neuraminidase deficiency in man. Proc. Natl. Acad. Sci. USA 79 (1982) 4535-4539
14. Tessitore A., del P Martin M., Sano R., Ma Y., Mann L., Ingrassia A., Laywell E.D., Steindler D.A., Hendershot L.M., and d'Azzo A. GM1-ganglioside-mediated activation of the unfolded protein response causes neuronal death in a neurodegenerative gangliosidosis. Mol. Cell. 15 (2004) 753-766
15. d'Azzo A., Tessitore A., and Sano R. Gangliosides as apoptotic signals in ER stress response. Cell. Death Differ. 13 (2006) 404-414
16. van der Voorn J.P., Kamphorst W., van der Knaap M.S., and Powers J.M. The leukoencephalopathy of infantile GM1 gangliosidosis: oligodendrocytic loss and axonal dysfunction. Acta Neuropathol. (Berl.) 107 (2004) 539-545
17. Folkerth R.D. Abnormalities of developing white matter in lysosomal storage diseases. J. Neuropathol. Exp. Neurol. 58 (1999) 887-902
18. Kaye E.M., Alroy J., Raghavan S.S., Schwarting G.A., Adelman L.S., Runge V., Gelblum D., Thalhammer J.G., and Zuniga G. Dysmyelinogenesis in animal model of GM1 gangliosidosis. Pediatr. Neurol. 8 (1992) 255-261
19. Jeyakumar M., Thomas R., Elliot-Smith E., Smith D.A., van der Spoel A.C., d'Azzo A., Perry V.H., Butters T.D., Dwek R.A., and Platt F.M. Central nervous system inflammation is a hallmark of pathogenesis in mouse models of GM1 and GM2 gangliosidosis. Brain 126 (2003) 974-987
20. Takamura A., Higaki K., Kajimaki K., Otsuka S., Ninomiya H., Matsuda J., Ohno K., Suzuki Y., and Nanba E. Enhanced autophagy and mitochondrial aberrations in murine G(M1)-gangliosidosis. Biochem. Biophys. Res. Commun. 367 (2008) 616-622
21. Hanson M., Lupski J.R., Hicks J., and Metry D. Association of dermal melanocytosis with lysosomal storage disease: clinical features and hypotheses regarding pathogenesis. Arch. Dermatol. 139 (2003) 916-920
22. Silengo M., Battistoni G., and Spada M. Is there a relationship between extensive mongolian spots and inborn errors of metabolism?. Am. J. Med. Genet. 87 (1999) 276-277
23. Tang T.T., Esterly N.B., Lubinsky M.S., Oechler H.W., Harb J.M., and Franciosi R.A. GM1-gangliosidosis type 1 involving the cutaneous vascular endothelial cells in a black infant with multiple ectopic Mongolian spots. Acta Derm. Venereol. 73 (1993) 412-415
24. Bloch L.D., Matsumoto F.Y., Belda Jr. W., Giugliani R., Menezes L.F., Kim C.A., and Machado M.C. Dermal melanocytosis associated with GM1-gangliosidosis type 1. Acta Derm. Venereol. 86 (2006) 156-158
25. Beratis N.G., Varvarigou-Frimas A., Beratis S., and Sklower S.L. Angiokeratoma corporis diffusum in GM1 gangliosidosis, type 1. Clin. Genet. 36 (1989) 59-64
26. Ishii N., Oshima A., Sakuraba H., Fukuyama Y., and Suzuki Y. Normal serum beta-galactosidase in juvenile GM1 gangliosidosis. Pediatr. Neurol. 10 (1994) 317-319
27. Callahan J.W. Molecular basis of GM1 gangliosidosis and Morquio disease, type B. Structure-function studies of lysosomal beta-galactosidase and the non-lysosomal beta-galactosidase-like protein. Biochim. Biophys. Acta 1455 (1999) 85-103
28. Okumiya T., Sakuraba H., Kase R., and Sugiura T. Imbalanced substrate specificity of mutant beta-galactosidase in patients with Morquio B disease. Mol. Genet. Metab. 78 (2003) 51-58
29. Oshima A., Tsuji A., Nagao Y., Sakuraba H., and Suzuki Y. Cloning, sequencing, and expression of cDNA for human beta-galactosidase. Biochem. Biophys. Res. Commun. 157 (1988) 238-244
30. Morreau H., Galjart N.J., Gillemans N., Willemsen R., van der Horst G.T., and d'Azzo A. Alternative splicing of beta-galactosidase mRNA generates the classic lysosomal enzyme and a beta-galactosidase-related protein. J. Biol. Chem. 264 (1989) 20655-20663
31. Privitera S., Prody C.A., Callahan J.W., and Hinek A. The 67-kDa enzymatically inactive alternatively spliced variant of beta-galactosidase is identical to the elastin/laminin-binding protein. J. Biol. Chem. 273 (1998) 6319-6326
32. Hinek A., Zhang S., Smith A.C., and Callahan J.W. Impaired elastic-fiber assembly by fibroblasts from patients with either Morquio B disease or infantile GM1-gangliosidosis is linked to deficiency in the 67-kD spliced variant of beta-galactosidase. Am. J. Hum. Genet. 67 (2000) 23-36
33. Caciotti A., Donati M.A., Boneh A., d'Azzo A., Federico A., Parini R., Antuzzi D., Bardelli T., Nosi D., Kimonis V., Zammarchi E., and Morrone A. Role of beta-galactosidase and elastin binding protein in lysosomal and nonlysosomal complexes of patients with GM1-gangliosidosis. Hum. Mutat. 25 (2005) 285-292
34. Morrone A., Bardelli T., Donati M.A., Giorgi M., Di Rocco M., Gatti R., Parini R., Ricci R., Taddeucci G., D'Azzo A., and Zammarchi E. Beta-galactosidase gene mutations affecting the lysosomal enzyme and the elastin-binding protein in GM1-gangliosidosis patients with cardiac involvement. Hum. Mutat. 15 (2000) 354-366
35. Chakraborty S., Rafi M.A., and Wenger D.A. Mutations in the lysosomal beta-galactosidase gene that cause the adult form of GM1 gangliosidosis. Am. J. Hum. Genet. 54 (1994) 1004-1113
36. Caciotti A., Bardelli T., Cunningham J., D'Azzo A., Zammarchi E., and Morrone A. Modulating action of the new polymorphism L436F detected in the GLB1 gene of a type-II GM1 gangliosidosis patient. Hum. Genet. 113 (2003) 44-50
37. Caciotti A., Donati M.A., Bardelli T., d'Azzo A., Massai G., Luciani L., Zammarchi E., and Morrone A. Primary and secondary elastin-binding protein defect leads to impaired elastogenesis in fibroblasts from GM1-gangliosidosis patients. Am. J. Pathol. 167 (2005) 1689-1698
38. Kooper A.J., Janssens P.M., de Groot A.N., Liebrand-van Sambeek M.L., van den Berg C.J., Tan-Sindhunata G.B., van den Berg P.P., Bijlsma E.K., Smits A.P., and Wevers R.A. Lysosomal storage diseases in non-immune hydrops fetalis pregnancies. Clin. Chim. Acta 371 (2006) 176-182
39. Yoshida K., Oshima A., Shimmoto M., Fukuhara Y., Sakuraba H., Yanagisawa N., and Suzuki Y. Human beta-galactosidase gene mutations in GM1-gangliosidosis: a common mutation among Japanese adult/chronic cases. Am. J. Hum. Genet. 49 (1991) 435-442
40. Chiu N.C., Qian W.H., Shanske A.L., Brooks S.S., and Boustany R.M. A common mutation site in the beta-galactosidase gene originates in Puerto Rico. Pediatr. Neurol. 14 (1996) 53-56
41. Nishimoto J., Nanba E., Inui K., Okada S., and Suzuki K. GM1-gangliosidosis (genetic beta-galactosidase deficiency): identification of four mutations in different clinical phenotypes among Japanese patients. Am. J. Hum. Genet. 49 (1991) 566-574
42. Boustany R.M., Qian W.H., and Suzuki K. Mutations in acid beta-galactosidase cause GM1-gangliosidosis in American patients. Am. J. Hum. Genet. 53 (1993) 881-888
43. Silva C.M., Severini M.H., Sopelsa A., Coelho J.C., Zaha A., d'Azzo A., and Giugliani R. Six novel beta-galactosidase gene mutations in Brazilian patients with GM1-gangliosidosis. Hum. Mutat. 13 (1999) 401-409
44. Gururaj A., Sztriha L., Hertecant J., Johansen J.G., Georgiou T., Campos Y., Drousiotou A., and d'Azzo A. Magnetic resonance imaging findings and novel mutations in GM1 gangliosidosis. J. Child. Neurol. 20 (2005) 57-60
45. Caciotti A., Donati M.A., Procopio E., Filocamo M., Kleijer W., Wuyts W., Blaumeiser B., d'Azzo A., Simi L., Orlando C., McKenzie F., Fiumara A., Zammarchi E., and Morrone A. GM1 gangliosidosis: molecular analysis of nine patients and development of an RT-PCR assay for GLB1 gene expression profiling. Hum. Mutat. 28 (2007) 204
46. Santamaria R., Blanco M., Chabas A., Grinberg D., and Vilageliu L. Identification of 14 novel GLB1 mutations, including five deletions, in 19 patients with GM1 gangliosidosis from South America. Clin. Genet. 71 (2007) 273-279
47. Kaye E.M., Shalish C., Livermore J., Taylor H.A., Stevenson R.E., and Breakefield X.O. Beta-galactosidase gene mutations in patients with slowly progressive GM1 gangliosidosis. J. Child Neurol. 12 (1997) 242-247
48. Zhang S., Bagshaw R., Hilson W., Oho Y., Hinek A., Clarke J.T., and Callahan J.W. Characterization of beta-galactosidase mutations Asp332 > Asn and Arg148 > Ser, and a polymorphism, Ser532 > Gly, in a case of GM1 gangliosidosis. Biochem. J. 348 Pt. 3 (2000) 621-632
49. Georgiou T., Drousiotou A., Campos Y., Caciotti A., Sztriha L., Gururaj A., Ozand P., Zammarchi E., Morrone A., and D'Azzo A. Four novel mutations in patients from the Middle East with the infantile form of GM1-gangliosidosis. Hum. Mutat. 24 (2004) 352
50. Oshima A., Yoshida K., Shimmoto M., Fukuhara Y., Sakuraba H., and Suzuki Y. Human beta-galactosidase gene mutations in morquio B disease. Am. J. Hum. Genet. 49 (1991) 1091-1093
51. Paschke E., Milos I., Kreimer-Erlacher H., Hoefler G., Beck M., Hoeltzenbein M., Kleijer W., Levade T., Michelakakis H., and Radeva B. Mutation analyses in 17 patients with deficiency in acid beta-galactosidase: three novel point mutations and high correlation of mutation W273L with Morquio disease type B. Hum. Genet. 109 (2001) 159-166
52. Ishii N., Oohira T., Oshima A., Sakuraba H., Endo F., Matsuda I., Sukegawa K., Orii T., and Suzuki Y. Clinical and molecular analysis of a Japanese boy with Morquio B disease. Clin. Genet. 48 (1995) 103-108
53. Brunetti-Pierri N., Mian A., Luetchke R., and Graham B.H. Intrauterine growth retardation and placental vacuolization as presenting features in a case of GM1 gangliosidosis. J. Inherit. Metab. Dis. 30 (2007) 823
54. Oshima A., Yoshida K., Ishizaki A., Shimmoto M., Fukuhara Y., Sakuraba H., and Suzuki Y. GM1-gangliosidosis: tandem duplication within exon 3 of beta-galactosidase gene in an infantile patient. Clin. Genet. 41 (1992) 235-238
55. Morrone A., Morreau H., Zhou X.Y., Zammarchi E., Kleijer W.J., Galjaard H., and d'Azzo A. Insertion of a T next to the donor splice site of intron 1 causes aberrantly spliced mRNA in a case of infantile GM1-gangliosidosis. Hum. Mutat. 3 (1994) 112-120
56. Hirayama M., Kitagawa Y., Yamamoto S., Tokuda A., Mutoh T., Hamano T., Aita T., and Kuriyama M. GM1 gangliosidosis type 3 with severe jaw-closing impairment. J. Neurol. Sci. 152 (1997) 99-101
57. Roze E., Paschke E., Lopez N., Eck T., Yoshida K., Maurel-Ollivier A., Doummar D., Caillaud C., Galanaud D., Billette de Villemeur T., Vidailhet M., and Roubergue A. Dystonia and parkinsonism in GM1 type 3 gangliosidosis. Mov. Disord. 20 (2005) 1366-1369
58. Bagshaw R.D., Zhang S., Hinek A., Skomorowski M.A., Whelan D., Clarke J.T., and Callahan J.W. Novel mutations (Asn 484 Lys, Thr 500 Ala, Gly 438 Glu) in Morquio B disease. Biochim. Biophys. Acta 1588 (2002) 247-253
59. Yoshida K., Ikeda S., Kawaguchi K., and Yanagisawa N. Adult GM1 gangliosidosis: immunohistochemical and ultrastructural findings in an autopsy case. Neurology 44 (1994) 2376-2382
60. Yoshida K., Oshima A., Sakuraba H., Nakano T., Yanagisawa N., Inui K., Okada S., Uyama E., Namba R., Iwasaki K., Kondo S., Takamiya K., and Suzuki Y. GM1 gangliosidosis in adults: clinical and molecular analysis of 16 Japanese patients. Ann. Neurol. 31 (1992) 328-332
61. K. Suzuki, H. Sakuraba, O. Akiro, β-galactosidase deficiency (β-galactosidosis): GM1-gangliosidosis and Morquio B disease, The Metabolic and Molecular Bases of Inherited Disease, McGraw-Hill, New York, 1995, pp. 2785-2823.
62. Hilson W.L., Okamura-Oho Y., Zhang S., Clarke J.T., Mahuran D., and Callahan J.W. Novel missense mutations in β-galactosidase that results in GM1-gangliosidosis. Am. J. Hum. Genet. 55 S3 (1994) 1302
63. Matsuda J., Suzuki O., Oshima A., Ogura A., Noguchi Y., Yamamoto Y., Asano T., Takimoto K., Sukegawa K., Suzuki Y., and Naiki M. Beta-galactosidase-deficient mouse as an animal model for GM1-gangliosidosis. Glycoconj. J. 14 (1997) 729-736
64. Hahn C.N., del Pilar Martin M., Schroder M., Vanier M.T., Hara Y., Suzuki K., Suzuki K., and d'Azzo A. Generalized CNS disease and massive GM1-ganglioside accumulation in mice defective in lysosomal acid beta-galactosidase. Hum. Mol. Genet. 6 (1997) 205-211
65. 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. Chemical chaperone therapy for brain pathology in G(M1)-gangliosidosis. Proc. Natl. Acad. Sci. USA 100 (2003) 15912-15917
66. Shield J.P., Stone J., and Steward C.G. Bone marrow transplantation correcting beta-galactosidase activity does not influence neurological outcome in juvenile GM1-gangliosidosis. J. Inherit. Metab. Dis. 28 (2005) 797-798
67. Kasperzyk J.L., d'Azzo A., Platt F.M., Alroy J., and Seyfried T.N. Substrate reduction reduces gangliosides in postnatal cerebrum-brainstem and cerebellum in GM1 gangliosidosis mice. J. Lipid Res. 46 (2005) 744-751
68. Kasperzyk J.L., El-Abbadi M.M., Hauser E.C., D'Azzo A., Platt F.M., and Seyfried T.N. N-butyldeoxygalactonojirimycin reduces neonatal brain ganglioside content in a mouse model of GM1 gangliosidosis. J. Neurochem. 89 (2004) 645-653
69. Takaura N., Yagi T., Maeda M., Nanba E., Oshima A., Suzuki Y., Yamano T., and Tanaka A. Attenuation of ganglioside GM1 accumulation in the brain of GM1 gangliosidosis mice by neonatal intravenous gene transfer. Gene. Ther. 10 (2003) 1487-1493
70. Broekman M.L., Baek R.C., Comer L.A., Fernandez J.L., Seyfried T.N., and Sena-Esteves M. Complete correction of enzymatic deficiency and neurochemistry in the GM1-gangliosidosis mouse brain by neonatal adeno-associated virus-mediated gene delivery. Mol. Ther. 15 (2007) 30-37
71. Suzuki Y., Ichinomiya S., Kurosawa M., Ohkubo M., Watanabe H., Iwasaki H., Matsuda J., Noguchi Y., Takimoto K., Itoh M., Tabe M., Iida M., Kubo T., Ogawa S., Nanba E., Higaki K., Ohno K., and Brady R.O. Chemical chaperone therapy: clinical effect in murine G(M1)-gangliosidosis. Annals Neurol. 62 (2007) 671-675
72. Satoh H., Yamato O., Asano T., Yamasaki M., and Maede Y. Increased concentration of GM1-ganglioside in cerebrospinal fluid in dogs with GM1- and GM2-gangliosidoses and its clinical application for diagnosis. J. Vet. Diagn. Invest. 16 (2004) 223-226
73. Brunetti-Pierri N., Bhattacharjee M.B., Wang Z.J., Zili C., Wenger D.A., Potocki L., Hunter J., and Scaglia F. Brain proton magnetic resonance spectroscopy and neuromuscular pathology in a patient with GM1 gangliosidosis. J. Child Neurol. 23 (2008) 73-78
74. Santamaria R., Chabas A., Callahan J.W., Grinberg D., and Vilageliu L. Expression and characterization of 14 GLB1 mutant alleles found in GM1-gangliosidosis and Morquio B patients. J. Lipid Res. 48 (2007) 2275-2282