Structural and clinical implications of amino acid substitutions in α-l-iduronidase: Insight into the basis of mucopolysaccharidosis type I

Molecular Genetics and Metabolism

Volumn 111, Issue 2, 2014, Pages 107-112

  Saito, Seiji ^a   Ohno, Kazuki ^b,e   Maita, Nobuo ^c   Sakuraba, Hitoshi ^d  

^a HOKKAIDO INFORMATION UNIVERSITY   (Japan)

^b NPO for the Promotion of Research on Intellectual Property Tokyo   (Japan)

^c UNIVERSITY OF TOKUSHIMA   (Japan)

^d MEIJI PHARMACEUTICAL UNIVERSITY   (Japan)

^e ASTELLAS PHARMA INC   (Japan)

Author keywords

l Iduronidase; Amino acid substitution; Mucopolysaccharidosis type I; Structural model

Indexed keywords

AMINO ACID; IMMUNOGLOBULIN; LEVO IDURONIDASE;

AMINO ACID SUBSTITUTION; ARTICLE; ATOM; CRYSTAL STRUCTURE; DISEASE ASSOCIATION; DISEASE SEVERITY; HUMAN; HURLER SYNDROME; MISSENSE MUTATION; MUTANT; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN STRUCTURE;

AMINO ACID SUBSTITUTION; MUCOPOLYSACCHARIDOSIS TYPE I; STRUCTURAL MODEL; Α-L-IDURONIDASE;

AMINO ACID SUBSTITUTION; CATALYTIC DOMAIN; GENE EXPRESSION; HUMANS; IDURONIDASE; MODELS, MOLECULAR; MUCOPOLYSACCHARIDOSIS I; MUTATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; SEVERITY OF ILLNESS INDEX; STRUCTURAL HOMOLOGY, PROTEIN; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84893696262     PISSN: 10967192     EISSN: 10967206     Source Type: Journal    
DOI: 10.1016/j.ymgme.2013.10.005     Document Type: Article

References (51)

1. Neufeld E.F., Muenzer J. The mucopolysaccharidoses. The metabolic and molecular bases of inherited disease 2001, 3421-3452. McGraw-Hill, New York. 8th edn. C.R. Scriver, A.L. Beaudet, W.S. Sly, D. Valle (Eds.).
2. Scott H.S., Ashton L.J., Eyre H.J., Backer E., Brooks D.A., Callen D.F., Sutherland G.R., Morris C.O., Hopwood J.J. Chromosomal localization of the human a-L-iduronidase (IDUA) to 4p16.3. Am. J. Hum. Genet. 1990, 47:802-807.
3. Scott H.S., Guo X.-H., Hopwood J.J., Morris C.P. Structure and sequence of the a-L-iduronidase gene. Genomics 1992, 13:1311-1313.
4. Tylor J.A., Gibson G.J., Brooks D.A., Hopwood J.J. α-L-iduronidase in normal and mucopolysaccharidosis type I human skin fibroblasts. Biochem. J. 1991, 274:263-268.
5. Brooks D.A. Review: the immunochemical analysis of enzyme from mucopolysaccharidoses patients. J. Inherit. Metab. Dis. 1993, 16:3-15.
6. Terlato N.J., Cox G.F. Can mucopolysaccharidosis type I disease severity be predicted based on a patient's genotype? A comprehensive review of the literature. Genet. Med. 2003, 5:286-294.
7. Pollard L.M., Jones J.R., Wood T.C. Molecular characterization of 355 mucopolysaccharidosis patients reveals 104 novel mutations. J. Inherit. Metab. Dis. 2013, 36:179-187.
8. Sugawara K., Saito S., Ohno K., Okuyama T., Sakuraba H. Structural study on mutant alpha-L-iduronidases: insight into mucopolysaccharidosis type I. J. Hum. Genet. 2008, 53:467-474.
9. Rempel B.P., Clarke L.A., Withers S.G. A homology model for human α-L-iduronidase: insights into human disease. Mol. Genet. Metab. 2005, 85:28-37.
10. Maita N., Tsukimura T., Taniguchi T., Saito S., Ohno K., Taniguchi H., Sakuraba H. Human α-L-iduronidase uses its own N-glycan as a substrate-binding and catalytic module. Proc. Natl. Acad. Sci. U. S. A. 2013, 110:14628-14633.
11. Taylor W.R. Protein structure comparison using iterated double dynamic programming. Protein Sci. 1999, 8:654-665.
12. McDonald I.K., Thornton J.M. Satisfying hydrogen bonding potential in proteins. J. Mol. Biol. 1994, 238:777-793.
13. Weiner S.J., Kallman P.A., Case D.A., Singh U.C., Ghio C., Alagona G., Profeta S., Weiner P. A new force field for molecular mechanical simulation of nucleic acids and proteins. J. Am. Chem. Soc. 1984, 106:765-784.
14. Kundrot C.E., Ponder J.W., Richards F.M. Algorithms for calculating excluded volume and its derivative as a function of molecular conformation and their use in energy minimization. J. Comput. Chem. 1991, 12:402-409.
15. Dudek M.J., Ponder J.W. Accurate modeling of the intramolecular electrostatic energy of proteins. J. Comput. Chem. 1995, 16:791-816.
16. Pappu R.V., Hart R.W., Ponder J.W. Analysis and application of potential energy smoothing for global optimization. J. Phys. Chem. B 1998, 102:9725-9742.
17. Ren P., Ponder J.W. Polarizable atomic multipole water model for molecular mechanics simulation. J. Phys. Chem. B 2003, 107:5933-5947.
18. Sakuraba H., Matsuzawa F., Aikawa S., Doi H., Kotani M., Lin H., Ohno K., Tanaka A., Yamada H., Uyama E. Molecular and structural studies of the GM2 gangliosidosis O variant. J. Hum. Genet. 2000, 47:176-183.
19. Sakuraba H., Matsuzawa F., Aikawa S., Doi H., Kotani M., Nakada H., Fukushige T., Kanzaki T. Structural and immunocytochemical studies on α-N-acetylgalactosaminidase deficiency (Schindler/Kanzaki disease). J. Hum. Genet. 2004, 49:1-8.
20. Matsuzawa F., Aikawa S., Sakuraba H., Lan H.T., Tanaka A., Ohno K., Sugimoto Y., Ninomiya H., Doi H. Structural basis of the GM2 gangliosidosis B variant. J. Hum. Genet. 2003, 48:582-589.
21. Matsuzawa F., Aikawa S., Doi H., Okumiya T., Sakuraba H. Fabry disease: correlation between structural changes in α-galactosidase, and clinical and biochemical phenotype. Hum. Genet. 2005, 117:317-328.
22. Bunge S., Kleijer W.J., Steglich C., Beck M., Zuther C., Morris C.P., Schwinger E., Hopwood J.J., Scott H.S., Gal A. Mucopolysaccharidosis type I: identification of 8 novel mutations and determination of the frequency of the two common alpha-L-iduronidase mutations (W402X and Q70X) among European patients. Hum. Mol. Genet. 1994, 3:861-866.
23. Clarke L.A., Nelson P.V., Warrington C.L., Morris C.P., Hopwood J.J., Scott H.S. Mutation analysis of 19 North American mucopolysaccharidosis type I patients: identification of two additional frequent mutations. Hum. Mutat. 1994, 3:275-282.
24. Bertola F., Filocamo M., Casati G., Mort M., Rosano C., Tylki-Szymanska A., Tüysüz B., Gabrielli O., Grossi S., Scarpa M., Parenti G., Antuzzi D., Dalmau J., Di Rocco M., Vici C.D., Okur I., Rosell J., Rovelli A., Furlan F., Rigoldi M., Biondi A., Cooper D.N., Parini R. IDUA mutational profiling of a cohort of 102 European patients with mucopolysaccharidosis type I: identification and characterization of 35 novel α-L-iduronidase (IDUA) alleles. Hum. Mutat. 2011, 32:E2189-E2210.
25. Venturi N., Rovelli A., Parini R., Menni F., Brambillasca F., Bertagnolio F., Uziel G., Gatti R., Filocamo M., Donati M.A., Biondi A., Goldwurm S. Molecular analysis of 30 mucopolysaccharidosis type I patients: evaluation of the mutational spectrum in Italian population and identification of 13 novel mutations. Hum. Mutat. 2002, 20:231.
26. Chkioua L., Khedhiri S., Turkia H.B., Tcheng R., Froissart R., Chahed H., Ferchichi S., Ben Dridi M.F., Vianey-Saban C., Laradi S., Miled A. Mucopolysaccharidosis type I: molecular characteristics of two novel alpha-L-iduronidase mutations in Tunisian patients. Diagn. Pathol. 2011, 6:47.
27. Wang X., Zhang W., Shi H., Qiu Z., Meng Y., Yao F., Wei M. Mucopolysaccharidosis I mutations in Chinese patients: identification of 27 novel mutations and 6 cases involving prenatal diagnosis. Clin. Genet. 2012, 81:443-452.
28. Brooks D.A., Fabrega S., Hein L.K., Parkinson E.J., Durand P., Yogalingam G., Matte U., Giugliani R., Dasvarma A., Eslahpazire J., Henrissat B., Mornon J.P., Hopwood J.J., Lehn P. Glycosidase active site mutations in human alpha-L-iduronidase. Glycobiology 2001, 11:741-750.
29. Beesley C.E., Meaney C.A., Greenland G., Adams V., Vellodi A., Young E.P., Winchester B.G. Mutational analysis of 85 mucopolysaccharidosis type I families: frequency of known mutations, identification of 17 novel mutations and in vitro expression of missense mutations. Hum. Genet. 2001, 109:503-511.
30. Li P., Wood T., Thompson J.N. Diversity of mutations and distribution of single nucleotide polymorphic alleles in the human alpha-L-iduronidase (IDUA) gene. Genet. Med. 2002, 4:420-426.
31. Laradi S., Tukel T., Erazo M., Shabbeer J., Chkioua L., Khedhiri S., Ferchichi S., Chaabouni M., Miled A., Desnick R.J. Mucopolysaccharidosis I: alpha-L-iduronidase mutations in three Tunisian families. J. Inherit. Metab. 2005, 28:1019-1026.
32. Scott H.S., Bunge S., Gal A., Clarke L.A., Morris C.P., Hopwood J.J. Molecular genetics of mucopolysaccharidosis type I: diagnostic, clinical, and biological implications. Hum. Mutat. 1995, 6:288-302.
33. Yogalingam G., Guo X.H., Muller V.J., Brooks D.A., Clements P.R., Kakkis E.D., Hopwood J.J. Identification and molecular characterization of alpha-L-iduronidase mutations present in mucopolysaccharidosis type I patients undergoing enzyme replacement therapy. Hum. Mutat. 2004, 24:199-207.
34. Bach G., Moskowitz S.M., Tieu P.T., Matynia A., Neufeld E.F. Molecular analysis of Hurler syndrome in Druze and Muslim Arab patients in Israel: multiple allelic mutations of the IDUA gene in a small geographic area. Am. J. Hum. Genet. 1993, 53:330-338.
35. Bartholomew D., McClellan J. A novel missense mutation in the human IDUA gene associated with a severe Hurler's phenotype. Hum. Mutat. 1998, 12:291.
36. Voskoboeva E.Y., Krasnopolskaya X.D., Mirenburg T.V., Weber B., Hopwood J.J. Molecular genetics of mucopolysaccharidosis type I: mutation analysis among the patients of the former Soviet Union. Mol. Genet. Metab. 1998, 65:174-180.
37. Vazna A., Beesley C., Berna L., Stolnaja L., Myskova H., Bouckova M., Vlaskova H., Poupetova H., Zeman J., Magner M., Hlavata A., Winchester B., Hrebicek M., Dvorakova L. Mucopolysaccharidosis type I in 21 Czech and Slovak patients: mutation analysis suggests a functional importance of C-terminus of the IDUA protein. Am. J. Med. Genet. A 2009, 149A:965-974.
38. Matte U., Yogalingam G., Brooks D., Leistner S., Schwartz I., Lima L., Norato D.Y., Brum J.M., Beesley C., Winchester B., Giugliani R., Hopwood J.J. Identification and characterization of 13 new mutations in mucopolysaccharidosis type I patients. Mol. Genet. Metab. 2003, 78:37-43.
39. Scott H.S., Litjens T., Nelson P.V., Brooks D.A., Hopwood J.J., Morris C.P. alpha-L-iduronidase mutations (Q70X and P533R) associate with a severe Hurler phenotype. Hum. Mutat. 1992, 1:333-339.
40. Clarke L.A., Scott H.S. Two novel mutations causing mucopolysaccharidosis type I detected by single strand conformational analysis of the alpha-L-iduronidase gene. Hum. Mol. Genet. 1993, 2:1311-1312.
41. Teng Y.N., Wang T.R., Hwu W.L., Lin S.P., Lee-Chen G.J. Identification and characterization of -3c-g acceptor splice site mutation in human alpha-L-iduronidase associated with mucopolysaccharidosis type IH/S. Clin. Genet. 2000, 57:131-136.
42. Sun L., Li C., Song X., Zheng N., Zhang H., Dong G. Three novel α-L-iduronidase mutations in 10 unrelated Chinese mucopolysaccharidosis type I families. Genet. Mol. Biol. 2011, 34:195-200.
43. Lee-Chen G.J., Wang T.R. Mucopolysaccharidosis type I: identification of novel mutations that cause Hurler/Scheie syndrome in Chinese families. J. Med. Genet. 1997, 34:939-941.
44. Tieu P.T., Bach G., Matynia A., Hwang M., Neufeld E.F. Four novel mutations underlying mild or intermediate forms of alpha-L-iduronidase deficiency (MPS IS and MPS IH/S). Hum. Mutat. 1995, 6:55-59.
45. Lee-Chen G.J., Lin S.P., Tang Y.F., Chin Y.W. Mucopolysaccharidosis type I: characterization of novel mutations affecting alpha-L-iduronidase activity. Clin. Genet. 1999, 56:66-70.
46. Dou W., Peng C., Zheng J.K., Gu X.F. A novel mutation of the alpha-L-iduronidase gene in a patient with mucopolysaccharidosis type I. Zhonghua Yi Xue Yi Chuan Xue Za Zhi 2007, 24:136-139. [Article in Chinese].
47. Prommajan K., Ausavarat S., Srichomthong C., Puangsricharern V., Suphapeetiporn K., Shotelersuk V. A novel p.E276K IDUA mutation decreasing α-L-iduronidase activity causes mucopolysaccharidosis type I. Mol. Vis. 2011, 17:456-460.
48. Oussoren E., Keulemans J., van Diggelen O.P., Oemardien L.F., Timmermans R.G., van der Ploeg A.T., Ruijter G.J. Residual α-L-iduronidase activity in fibroblasts of mild to severe mucopolysaccharidosis type I patients. Mol. Genet. Metab. 2013, 109:377-381.
49. Furukawa Y., Hamaguchi A., Nozaki I., Iizuka T., Sasagawa T., Shima Y., Demura S., Murakami H., Kawahara N., Okuyama T., Iwasa K., Yamada M. Cervical pachymeningeal hypertrophy as the initial and cardinal manifestation of mucopolysaccharidosis type I in monozygotic twins with a novel mutation in the alpha-L-iduronidase gene. Neurol. Sci. 2011, 302:121-125.
50. Bunge S., Kleijer W.J., Steglich C., Beck M., Schwinger E., Gal A. Mucopolysaccharidosis type I: identification of 13 novel mutations of the alpha-L-iduronidase gene. Hum. Mutat. 1995, 6:91-94.
51. Chkioua L., Khedhiri S., Kassab A., Bibi A., Ferchichi S., Froissart R., Vianey-Saban C., Laradi S., Miled A. Molecular analysis of mucopolysaccharidosis type I in Tunisia: identification of novel mutation and eight Novel polymorphisms. Diagn. Pathol. 2011, 6:39.