SUMF1 mutations affecting stability and activity of formylglycine generating enzyme predict clinical outcome in multiple sulfatase deficiency

European Journal of Human Genetics

Volumn 19, Issue 3, 2011, Pages 253-261

  Schlotawa, Lars ^a   Ennemann, Eva Charlotte ^b   Radhakrishnan, Karthikeyan ^b   Schmidt, Bernhard ^a   Chakrapani, Anupam ^c   Christen, Hans Jürgen ^d   Moser, Hugo ^e   Steinmann, Beat ^f   Dierks, Thomas ^b   Gärtner, Jutta ^a  

^a UNIVERSITY OF GÖTTINGEN   (Germany)

^b BIELEFELD UNIVERSITY   (Germany)

^c BIRMINGHAM CHILDREN S HOSPITAL   (United Kingdom)

^d Children's Hospital Auf der Bult   (Germany)

^e JOHNS HOPKINS UNIVERSITY   (United States)

^f UNIVERSITY CHILDREN S HOSPITAL   (Switzerland)

Author keywords

formylglycine generating enzyme; genotype phenotype correlation; lysosomal storage disorders; multiple sulfatase deficiency; sulfatase; SUMF1

Indexed keywords

ENZYME; FORMYLGLYCINE GENERATING ENZYME; SULFATASE; SULFATASE MODIFYING FACTOR 1; UNCLASSIFIED DRUG;

ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE COURSE; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME STABILITY; GENE MUTATION; GENETIC COUNSELING; HUMAN; MISSENSE MUTATION; MULTIPLE SULFATASE DEFICIENCY; NEWBORN; NONSENSE MUTATION; OUTCOME ASSESSMENT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STABILITY;

AGE OF ONSET; CATALYTIC DOMAIN; CHILD, PRESCHOOL; CODON, NONSENSE; FIBROBLASTS; GENETIC ASSOCIATION STUDIES; HUMANS; INFANT; INFANT, NEWBORN; LYSOSOMAL STORAGE DISEASES; MULTIPLE SULFATASE DEFICIENCY DISEASE; MUTATION, MISSENSE; PHENOTYPE; SULFATASES;

EID: 79951811108     PISSN: 10184813     EISSN: 14765438     Source Type: Journal    
DOI: 10.1038/ejhg.2010.219     Document Type: Article

References (45)

1. Hopwood J, Ballabio A: Multiple sulfatase deficiency and the nature of the sulfatase family. in Scriver CR BA, Valle D, Sly WS (eds): The Metabolic and Molecular Bases of Inherited Disease. New York: McGraw-Hill, 2001, pp 3725-3732.
2. Nyhan WL, Ozand PT: Atlas of Metabolic Diseases. London: Chapman and Hall Medical, 1998, pp 614-621.
3. Van Der Knaap M, Valk J: Magnetic Resonance of Myelination and Myelin Disorders, 3 edn, Berlin, Heidelberg, New York: Springer, 2005, pp 82-86.
4. Eto Y, Gomibuchi I, Umezawa F, Tsuda T: Pathochemistry, pathogenesis and enzyme replacement in multiple-sulfatase deficiency. Enzyme 1987; 38: 273-279. (Pubitemid 18001046)
5. Perlmutter-Cremer N, Libert J, Vamos E, Spehl M, Liebaers I: Unusual early manifestation of multiple sulfatase deficiency. Ann Radiol (Paris) 1981; 24: 43-48. (Pubitemid 11176836)
6. Vamos E, Liebaers I, Bousard N, Libert J, Perlmutter N: Multiple sulphatase deficiency with early onset. J Inherit Metab Dis 1981; 4: 103-104. (Pubitemid 11038421)
7. Burch M, Fensom AH, Jackson M, Pitts-Tucker T, Congdon PJ: Multiple sulphatase deficiency presenting at birth. Clin Genet 1986; 30: 409-415. (Pubitemid 17200190)
8. Busche A, Hennermann JB, Burger F et al: Neonatal manifestation of multiple sulfatase deficiency. Eur J Pediatr 2009; 168: 969-973.
9. Diaz-Font A, Santamaria R, Cozar M et al: Clinical and mutational characterization of three patients with multiple sulfatase deficiency: report of a new splicing mutation. Mol Genet Metab 2005; 86: 206-211. (Pubitemid 41412177)
10. Dierks T, Schlotawa L, Frese MA, Radhakrishnan K, von Figura K, Schmidt B: Molecular basis of multiple sulfatase deficiency, mucolipidosis II/III and Niemann-Pick C1 disease - Lysosomal storage disorders caused by defects of non-lysosomal proteins. Biochim Biophys Acta 2009; 1793: 710-725.
11. Mancini GM, Van Diggelen OP, Huijmans JG, Stroink H, de Coo RF: Pitfalls in the diagnosis of multiple sulfatase deficiency. Neuropediatrics 2001; 32: 38-40. (Pubitemid 32290433)
12. Loffeld A, Gray RG, Green SH, Roper HP, Moss C: Mild ichthyosis in a 4-year-old boy with multiple sulphatase deficiency. British J Dermatol 2002; 147: 353-355.
13. Schlotawa L, Steinfeld R, von Figura K, Dierks T, Gartner J: Molecular analysis of SUMF1 mutations: stability and residual activity of mutant formylglycine-generating enzyme determine disease severity in multiple sulfatase deficiency. Hum Mutat 2008; 29: 205.
14. Al Aqeel A, Ozand PT, Brismar J et al: Saudi variant of multiple sulfatase deficiency. J Child Neurol 1992; 7(Suppl): S12-S21.
15. Blanco-Aguirre ME, Kofman-Alfaro SH, Rivera-Vega MR et al: Unusual clinical presentation in two cases of multiple sulfatase deficiency. Pediatr Dermatol 2001; 18: 388-392. (Pubitemid 33070703)
16. Diez-Roux G, Ballabio A: Sulfatases and human disease. Annu Rev Genomics Hum Genet 2005; 6: 355-379. (Pubitemid 41397088)
17. Dierks T, Schmidt B, von Figura K: Conversion of cysteine to formylglycine: a protein modification in the endoplasmic reticulum. Proc Natl Acad Sci USA 1997; 94: 11963-11968. (Pubitemid 27467825)
18. Schmidt B, Selmer T, Ingendoh A, von Figura K: A novel amino acid modification in sulfatases that is defective in multiple sulfatase deficiency. Cell 1995; 82: 271-278.
19. Dierks T, Lecca MR, Schlotterhose P, Schmidt B, von Figura K: Sequence determinants directing conversion of cysteine to formylglycine in eukaryotic sulfatases. EMBO J 1999; 18: 2084-2091. (Pubitemid 29179166)
20. Dierks T, Dickmanns A, Preusser-Kunze A et al: Molecular basis for multiple sulfatase deficiency and mechanism for formylglycine generation of the human formylglycine-generating enzyme. Cell 2005; 121: 541-552. (Pubitemid 40720008)
21. Mariappan M, Radhakrishnan K, Dierks T, Schmidt B, von Figura K: ERp44 mediates a thiol-independent retention of formylglycine-generating enzyme in the endoplasmic reticulum. J Biol Chem 2008; 283: 6375-6383.
22. Cosma MP, Pepe S, Annunziata I et al: The multiple sulfatase deficiency gene encodes an essential and limiting factor for the activity of sulfatases. Cell 2003; 113: 445-456. (Pubitemid 36588748)
23. Dierks T, Schmidt B, Borissenko LV et al: Multiple sulfatase deficiency is caused by mutations in the gene encoding the human C(alpha)-formylglycine generating enzyme. Cell 2003; 113: 435-444. (Pubitemid 36588747)
24. Settembre C, Annunziata I, Spampanato C et al: Systemic inflammation and neuro-degeneration in a mouse model of multiple sulfatase deficiency. Proc Natl Acad Sci USA 2007; 104: 4506-4511. (Pubitemid 47186255)
25. Annunziata I, Bouche V, Lombardi A, Settembre C, Ballabio A: Multiple sulfatase deficiency is due to hypomorphic mutations of the SUMF1 gene. Hum Mutat 2007; 28: 928.
26. Cosma MP, Pepe S, Parenti G et al: Molecular and functional analysis of SUMF1 mutations in multiple sulfatase deficiency. Hum Mutat 2004; 23: 576-581. (Pubitemid 38720609)
27. Artigalas OA, da Silva LR, Burin M et al: Multiple sulfatase deficiency: clinical report and description of two novel mutations in a Brazilian patient. Metabolic brain disease 2009; 24: 493-500.
28. Steinmann B, Mieth D, Gitzelmann R: A newly recognized cause of low urinary estriol in pregnancy: multiple sulfatase deficiency of the fetus. Gynecol Obstet Invest 1981; 12: 107-109. (Pubitemid 11191278)
29. Preusser-Kunze A, Mariappan M, Schmidt B et al: Molecular characterization of the human Calpha-formylglycine-generating enzyme. J Biol Chem 2005; 280: 14900-14910. (Pubitemid 40562840)
30. Rommerskirch W, von Figura K: Multiple sulfatase deficiency: catalytically inactive sulfatases are expressed from retrovirally introduced sulfatase cDNAs. Proc Natl Acad Sci USA 1992; 89: 2561-2565.
31. Voznyi YV, Keulemans JL, Van Diggelen OP: A fluorimetric enzyme assay for the diagnosis of II MPS (Hunter disease). J Inherit Metab Dis 2001; 24: 675-680. (Pubitemid 33130088)
32. Gieselmann V, Schmidt B, von Figura K: In vitro mutagenesis of potential N-glycosyl-ation sites of arylsulfatase. A effects on glycosylation, phosphorylation, and intra-cellular sorting. J Biol Chem 1992; 267: 13262-13266.
33. Mariappan M, Gande SL, Radhakrishnan K, Schmidt B, Dierks T, von Figura K: The non-catalytic N-terminal extension of formylglycine-generating enzyme is required for its biological activity and retention in the endoplasmic reticulum. J Biol Chem 2008; 283: 11556-11564.
34. Roeser D, Preusser-Kunze A, Schmidt B et al: A general binding mechanism for all human sulfatases by the formylglycine-generating enzyme. Proc Natl Acad Sci USA 2006; 103: 81-86. (Pubitemid 43076108)
35. Fey J, Balleininger M, Borissenko LV, Schmidt B, von Figura K, Dierks T: Characterization of posttranslational formylglycine formation by luminal components of the endoplasmic reticulum. J Biol Chem 2001; 276: 47021-47028.
36. Vembar SS, Brodsky JL: One step at a time: endoplasmic reticulum-associated degradation. Nat Rev Mol Cell Biol 2008; 9: 944-957.
37. Christis C, Lubsen NH, Braakman I: Protein folding includes oligomerization - examples from the endoplasmic reticulum and cytosol. FEBS J 2008; 275: 4700-4727.
38. Fraldi A, Zito E, Annunziata F et al: Multistep, sequential control of the trafficking and function of the multiple sulfatase deficiency gene product, SUMF1 by PDI, ERGIC-53 and ERp44. Hum Mol Genet 2008; 17: 2610-2621.
39. Zito E, Buono M, Pepe S et al: Sulfatase modifying factor 1 trafficking through the cells: from endoplasmic reticulum to the endoplasmic reticulum. EMBO J 2007; 26: 2443-2453. (Pubitemid 46788321)
40. Peng J, Schmidt B, von Figura K, Dierks T: Identification of formylglycine in sulfatases by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. J Mass Spectrom 2003; 38: 80-86. (Pubitemid 36157760)
41. Conary JT, Hasilik A, von Figura K: Synthesis and stability of steroid sulfatase in fibroblasts from multiple sulfatase deficiency. Biol Chem Hoppe Seyler 1988; 369: 297-302.
42. Steckel F, Hasilik A, von Figura K: Multiple sulfatase deficiency: degradation of arylsulfatase A and B after endocytosis in fibroblasts. Eur J Biochem 1985; 151: 147-152. (Pubitemid 15226654)
43. Steckel F, Hasilik A, von Figura K: Synthesis and stability of arylsulfatase A and B in fibroblasts from multiple sulfatase deficiency. Eur J Biochem 1985; 151: 141-145. (Pubitemid 15226653)
44. Sawkar AR, Adamski-Werner SL, Cheng WC et al: Gaucher disease-associated glucocerebrosidases show mutation-dependent chemical chaperoning profiles. Chem Biol 2005; 12: 1235-1244. (Pubitemid 41628259)
45. Ulloa-Aguirre A, Janovick JA, Brothers SP, Conn PM: Pharmacologic rescue of conformationally-defective proteins: implications for the treatment of human disease. Traffic 2004; 5: 821-837. (Pubitemid 39433553)