Impact of β-galactosidase mutations on the expression of the canine lysosomal multienzyme complex

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1792, Issue 10, 2009, Pages 982-987

  Kreutzer, Robert ^a   Kreutzer, Mihaela ^a   Sewell, Adrian C ^b   Techangamsuwan, Somporn ^a   Leeb, Tosso ^c   Baumgärtner, Wolfgang ^a  

^a UNIVERSITY OF VETERINARY MEDICINE HANNOVER   (Germany)

^b UNIVERSITY HOSPITAL FRANKFURT   (Germany)

^c UNIVERSITY OF BERN   (Switzerland)

Author keywords

galactosidase variant; Differential expression; GM1 gangliosidosis; Lysosomal multienzyme complex; Neuraminidase 1; Protective protein cathepsin A

Indexed keywords

BETA GALACTOSIDASE; LYSOSOME ENZYME; MULTIENZYME COMPLEX; SIALIDASE;

ALLELE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DOG; ENZYME ACTIVITY; ENZYME ASSAY; ENZYME REGULATION; FIBROBLAST; GENE EXPRESSION; GENE MUTATION; GENOTYPE; GM1 GANGLIOSIDOSIS; HETEROZYGOSITY; HOMOZYGOSITY; LYSOSOME; LYSOSOME STORAGE DISEASE; MOLECULAR MECHANICS; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WESTERN BLOTTING;

ANIMALS; BETA-GALACTOSIDASE; CATHEPSIN A; DOGS; FIBROBLASTS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; LYSOSOMES; MULTIENZYME COMPLEXES; MUTATION; NEURAMINIDASE; RNA, MESSENGER;

EID: 70349287541     PISSN: 09254439     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbadis.2009.07.004     Document Type: Article

References (48)

1. Stalder L., and Mühlemann O. The meaning of nonsense. Trends Cell Biol. 18 (2008) 315-321
2. Wang Z.H., Zeng B., Shibuya H., Johnson G.S., Alroy J., Pastores G.M., Raghavan S., and Kolodny E.H. Isolation and characterization of the normal canine beta-galactosidase gene and its mutation in a dog model of GM1-gangliosidosis. J. Inherit. Metab. Dis. 23 (2000) 593-606
3. Yamato O., Endoh D., Kobayashi A., Masuoka Y., Yonemura M., Hatakeyama A., Satoh H., Tajima M., Yamasaki M., and Maede Y. A novel mutation in the gene for canine acid beta-galactosidase that causes GM1-gangliosidosis in Shiba dogs. Inherit. Metab. Dis. 25 (2002) 525-526
4. 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
5. Weatherall D.J. Phenotype-genotype relationships in monogenic disease: lessons from the thalassaemias. Nat. Rev. Genet. 2 (2001) 245-255
6. Cutting G.R. Modifier genetics: cystic fibrosis. Annu. Rev. Genomics Hum. Genet. 2005 6 (2005) 237-260
7. Rossetti S., and Harris P.C. Genotype-phenotype correlations in autosomal dominant and autosomal recessive polycystic kidney disease. Am. Soc. Nephrol. 18 (2007) 1374-1380
8. Iborra F.J., Escargueil A.E., Kwek K.Y., Akoulitchev A., and Cook P.R. Molecular cross-talk between the transcription, translation, and nonsense-mediated decay machineries. J. Cell Sci. 117 (2004) 899-906
9. Shyu A.B., Wilkinson M.F., and van Hoof A. Messenger RNA regulation: to translate or to degrade. EMBO J. 27 (2008) 471-481
10. Santamaria R., Chabás 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
11. Brunetti-Pierri N., and Scaglia F. GM(1) gangliosidosis: review of clinical, molecular, and therapeutic aspects. Mol. Genet. Metab. 94 (2008) 391-396
12. Santamaria R., Blanco M., Chabás 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
13. Trojak J.E., Ho C.K., Roesel R.A., Levin L.S., Kopits S.E., Thomas G.H., and Toma S. Morquio-like syndrome (MPS IV B) associated with deficiency of a beta-galactosidase. Johns Hopkins Med. J. 146 (1980) 75-79
14. Hinek A., Rabinovitch M., Keeley F., Okamura-Oho Y., and Callahan J. The 67-kD elastin/laminin-binding protein is related to an enzymatically inactive, alternatively spliced form of beta-galactosidase. J. Clin. Invest. 91 (1993) 1198-1205
15. 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
16. Yamato O., Masuoka Y., Yonemura M., Hatakeyama A., Satoh H., Kobayashi A., Nakayama M., Asano T., Shoda T., Yamasaki M., Ochiai K., Umemura T., and Maede Y. Clinical and clinico-pathologic characteristics of Shiba dogs with a deficiency of lysosomal acid beta-galactosidase: a canine model of human GM1 gangliosidosis. J. Vet. Med. Sci. 65 (2003) 213-217
17. Kreutzer R., Leeb T., G Müller A., Moritz W., and Baumgärtner A. duplication in the canine beta-galactosidase gene GLB1 causes exon skipping and GM1-gangliosidosis in Alaskan huskies. Genetics 170 (2005) 1857-1861
18. Kreutzer R., Kreutzer M., Pröpsting M.J., Sewell A.C., Leeb T., Naim H.Y., and Baumgärtner W. Insights into post-translational processing of beta-galactosidase in an animal model resembling late infantile human G-gangliosidosis. J. Cell. Mol. Med. 12 (2008) 1661-1671
19. Suzuki Y., Sakuraba H., Oshima A., Yoshida K., Shimmoto M., Takano T., and Fukuhara Y. Clinical and molecular heterogeneity in hereditary beta-galactosidase deficiency. Dev. Neurosci. 13 (1991) 299-303
20. Yoshida K., Oshima A., Sakuraba H., Nakano T., Yanagisawa N., Inui K., Okada S., Uyama E., Namba R., and Kondo K. GM1 gangliosidosis in adults: clinical and molecular analysis of 16 Japanese patients. Ann. Neurol. 31 (1992) 328-332
21. Santamaria R., Chabás 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
22. Nagy E., and Maquat L.E. A rule for termination-codon position within intron-containing genes: when nonsense affects RNA abundance. Trends Biochem. Sci. 23 (1998) 198-199
23. Asselta R., Duga S., Spena S., Santagostino E., Peyvandi F., Piseddu G., Targhetta R., Malcovati M., Mannucci P.M., and Tenchini M.L. Congenital afibrinogenemia: mutations leading to premature termination codons in fibrinogen A alpha-chain gene are not associated with the decay of the mutant mRNAs. Blood 98 (2001) 3685-3692
24. Lualdi S., Pittis M.G., Regis S., Parini R., Allegri A.E., Furlan F., Bembi B., and Filocamo M. Multiple cryptic splice sites can be activated by IDS point mutations generating misspliced transcripts. J. Mol. Med. 84 (2006) 692-700
25. Pshezhetsky A.V., and Potier M. Stoichiometry of the human lysosomal carboxypeptidase-beta-galactosidase complex. Biochem. Biophys. Res. Commun. 195 (1993) 354-362
26. Pshezhetsky A.V., and Potier M. Association of N-acetylgalactosamine-6-sulfate sulfatase with the multienzyme lysosomal complex of beta-galactosidase, cathepsin A, and neuraminidase. Possible implication for intralysosomal catabolism of keratan sulfate. J. Biol. Chem. 271 (1996) 28359-28365
27. Pshezhetsky A.V., and Ashmarina M. Lysosomal multienzyme complex: biochemistry, genetics, and molecular pathophysiology. Prog. Nucleic Acid Res. Mol. Biol. 69 (2001) 81-114
28. Hiraiwa M. Cathepsin A/protective protein: an unusual lysosomal multifunctional protein. Cell. Mol. Life Sci. 56 (1999) 894-907
29. Dimri G.P., Lee X., Basile G., Acosta G.M., Scott G., Roskelley C., Medrano E.E., Linskens M., Rubelj I., Pereira-Smith O., Peacocke M., and Campisi J. A biomarker that identifies senescent human cells in culture and in aging skin in vivo. Proc. Natl. Acad. Sci. U. S. A. 92 (1995) 9363-9367
30. Lee B.Y., Han J.A., Im J.S., Morrone A., Johung K., Goodwin E.C., Kleijer W.J., DiMaio D., and Hwang E.S. Senescence-associated beta-galactosidase is lysosomal beta-galactosidase. Aging Cell 5 (2006) 187-195
31. Kreutzer R., Müller G., Leeb T., Brenig B., Moritz A., and Baumgärtner W. Genetic testing for GM1-gangliosidosis in the Alaskan Husky. Tierärztl. Prax. 35 K (2007) 193-199
32. Kreutzer R., Kreutzer M., Leeb T., and Baumgärtner W. Rapid and accurate GM1-gangliosidosis diagnosis using a parentage testing microsatellite. Mol. Cell. Probes 22 (2008) 252-254
33. Müller G., Baumgärtner W., Moritz A., Sewell A., and Kustermann-Kuhn B. Biochemical findings in a breeding colony of Alaskan Huskies suffering from GM1-gangliosidosis. J. Inherit. Metab. Dis. 21 (1998) 430-431
34. Müller G., Alldinger S., Moritz A., Zurbriggen A., Kirchhof N., Sewell A., and Baumgärtner W. GM1-gangliosidosis in Alaskan huskies: clinical and pathologic findings. Vet. Pathol. 38 (2001) 281-290
35. Rozen S., and Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol. Biol. 132 (2000) 365-386
36. Pérez C., Vandesompele J., Vandenbroucke I., Holtappels G., Speleman F., Gevaert P., Van Cauwenberge P., and Bachert C. Quantitative real time polymerase chain reaction for measurement of human interleukin-5 receptor alpha spliced isoforms mRNA. BMC Biotechnol. 3 (2003) 17
37. Drögemüller C., Giese A., Martins-Wess F., Wiedemann S., Andersson L., Brenig B., Fries R., and Leeb T. The mutation causing the black-and-tan pigmentation phenotype of Mangalitza pigs maps to the porcine ASIP locus but does not affect its coding sequence. Mamm. Genome 17 (2006) 58-66
38. Ståhlberg A., Elbing K., Andrade-Garda J.M., Sjögreen B., Forootan A., Kubista M., and Multiway real-time P.C.R. gene expression profiling in yeast Saccharomyces cerevisiae reveals altered transcriptional response of ADH-genes to glucose stimuli. BMC Genomics 9 (2008) 170
39. Ponce E., Witte D.P., Hirschhorn R., Huie M.L., and Grabowski G.A. Murine acid alpha-glucosidase: cell-specific mRNA differential expression during development and maturation. Am. J. Pathol. 154 (1999) 1089-1096
40. Burrow T.A., Hopkin R.J., Leslie N.D., Tinkle B.T., and Grabowski G.A. Enzyme reconstitution/replacement therapy for lysosomal storage diseases. Curr. Opin. Pediatr. 19 (2007) 628-635
41. Erickson A.H., and Bocock J.P. Targeting to lysosomes in mammalian cells: the biosynthetic and endocytic pathways. Methods Mol Biol. 390 (2007) 339-361
42. Martin D.R., Rigat B.A., Foureman P., Varadarajan G.S., Hwang M., Krum B.K., Smith b.F., Callahan J.W., Mahuran D.J., and Baker H.J. Molecular consequences of the pathogenic mutation in feline GM1 gangliosidosis. Mol. Genet. Metab. 94 (2008) 212-221
43. Isken O., Kim Y.K., Hosoda N., Mayeur G.L., Hershey J.W., and Maquat L.E. Upf1 phosphorylation triggers translational repression during nonsense-mediated mRNA decay. Cell 133 (2008) 314-327
44. Potier M., Michaud L., Tranchemontagne J., and Thauvette L. Structure of the lysosomal neuraminidase-beta-galactosidase-carboxypeptidase multienzymic complex. Biochem. J. 267 (1990) 197-202
45. Ostrowska H., Krukowska K., Kalinowska J., Orłowska M., and Lengiewicz I. Lysosomal high molecular weight multienzyme complex. Cell. Mol. Biol. Lett. 2003 8 (2003) 19-24
46. Sergi C., Penzel R., Uhl J., Zoubaa S., Dietrich H., Decker N., Rieger P., Kopitz J., Otto H.F., Kiessling M., and Cantz M. Prenatal diagnosis and fetal pathology in a Turkish family harboring a novel nonsense mutation in the lysosomal alpha-N-acetyl-neuraminidase (sialidase) gene. Hum. Genet. 109 (2001) 421-428
47. Rottier R.J., Hahn C.N., Mann L.W., del Pilar Martin M., Smeyne R.J., Suzuki K., and d'Azzo A. Lack of PPCA expression only partially coincides with lysosomal storage in galactosialidosis mice: indirect evidence for spatial requirement of the catalytic rather than the protective function of PPCA. Hum. Mol. Genet. 7 (1998) 1787-1794
48. D'Agrosa R.M., Hubbes M., Zhang S., Shankaran R., and Callahan J.W. Characteristics of the beta-galactosidase-carboxypeptidase complex in GM1-gangliosidosis and beta-galactosialidosis fibroblasts. Biochem J. 285 (1992) 833-838