Optimizing the molecular diagnosis of GALNS: Novel methods to define and characterize morquio-A syndrome-associated mutations

Human Mutation

Volumn 36, Issue 3, 2015, Pages 357-368

  Caciotti, Anna ^a   Tonin, Rodolfo ^a,b   Rigoldi, Miriam ^c   Ferri, Lorenzo ^a,b   Catarzi, Serena ^a   Cavicchi, Catia ^a   Procopio, Elena ^a   Donati, Maria Alice ^a   Ficcadenti, Anna ^d   Fiumara, Agata ^e   Barone, Rita ^e   Garavelli, Livia ^f   Rocco, Maja Di ^g   Filocamo, Mirella ^g   Antuzzi, Daniela ^h   Scarpa, Maurizio ⁱ   Mooney, Sean D ^j   Li, Biao ^j   Skouma, Anastasia ^k   Bianca, Sebastiano ^l   Concolino, Daniela ^m   Casalone, Rosario ⁿ   Monti, Elena ^o,p   Pantaleo, Marilena ^a   Giglio, Sabrina ^a   Guerrini, Renzo ^a,b   Parini, Rossella ^c   Morrone, Amelia ^a,b   more..

^a UNIVERSITY OF FLORENCE   (Italy)

^b UNIVERSITY OF FLORENCE   (Italy)

^c SAN GERARDO HOSPITAL   (Italy)

^d Salesi Children's Hospital   (Italy)

^e UNIVERSITY OF CATANIA   (Italy)

^f S Maria Nuova Hospital Reggio   (Italy)

^g G GASLINI INSTITUTE   (Italy)

^h CATHOLIC UNIVERSITY   (Italy)

ⁱ UNIVERSITY HOSPITAL OF PADOVA   (Italy)

^j BUCK INSTITUTE FOR RESEARCH ON AGING   (United States)

^k UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

^l AO Garibaldi Nesima   (Italy)

^m UNIVERSITY MAGNA GRAECIA OF CATANZARO   (Italy)

ⁿ OSPEDALE DI CIRCOLO   (Italy)

^o QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^p UNIVERSITY OF VERONA   (Italy)

more..

Author keywords

GALNS; Intellectual disability; Morquio A; MPSIVA; Submicroscopic deletions

Indexed keywords

ARTICLE; BIOCHEMICAL COMPOSITION; CHILD; CLINICAL ARTICLE; COMPUTER MODEL; COPY NUMBER VARIATION; EXON; FEMALE; GENE; GENE DELETION; GENETIC ASSOCIATION; GENETIC DISORDER; GENOTYPE PHENOTYPE CORRELATION; HETEROZYGOSITY LOSS; HUMAN; HUMAN CELL; INTRON; ITALIAN (CITIZEN); LIVE BIRTH; MISSENSE MUTATION; MOLECULAR DIAGNOSIS; MORQUIO SYNDROME; N ACETYLGALACTOSAMINE 6 SULFATASE GENE; POLYMERASE CHAIN REACTION; PRESCHOOL CHILD; PRIORITY JOURNAL; SEQUENCE ANALYSIS; ADOLESCENT; ADULT; CELL LINE; CHEMISTRY; CYTOLOGY; FIBROBLAST; GENETICS; LYMPHOCYTE; MALE; MUCOPOLYSACCHARIDOSIS IV; MUTATION; PHENOTYPE; PROGNOSIS; SKIN; YOUNG ADULT;

IVA;

GALNS PROTEIN, HUMAN; ISOPROTEIN; MESSENGER RNA; N ACETYLGALACTOSAMINE 4 SULFATASE;

ADOLESCENT; ADULT; CELL LINE; CHONDROITINSULFATASES; FEMALE; FIBROBLASTS; HUMANS; LYMPHOCYTES; MALE; MUCOPOLYSACCHARIDOSIS IV; MUTATION; PHENOTYPE; PROGNOSIS; PROTEIN ISOFORMS; RNA, MESSENGER; SKIN; YOUNG ADULT;

EID: 84924558004     PISSN: 10597794     EISSN: 10981004     Source Type: Journal    
DOI: 10.1002/humu.22751     Document Type: Article

References (59)

1. Albuisson J, Murthy SE, Bandell M, Coste B, Louis-Dit-Picard H, Mathur J, Feneant-Thibault M, Tertian G, de Jaureguiberry JP, Syfuss PY, Cahalan S, Garcon L, et al. 2013. Dehydrated hereditary stomatocytosis linked to gain-of-function mutations in mechanically activated PIEZO1 ion channels. Nat Commun 4:1884.
2. Andolfo I, Alper SL, De Franceschi L, Auriemma C, Russo R, De Falco L, Vallefuoco F, Esposito MR, Vandorpe DH, Shmukler BE, Narayan R, Montanaro D, et al. 2013. Multiple clinical forms of dehydrated hereditary stomatocytosis arise from mutations in PIEZO1. Blood 121:3925-3935, S1-S12.
3. Bae C, Gnanasambandam R, Nicolai C, Sachs F, Gottlieb PA. 2013. Xerocytosis is caused by mutations that alter the kinetics of the mechanosensitive channel PIEZO1. Proc Natl Acad Sci USA 110:E1162-E1168.
4. Baker E, Guo XH, Orsborn AM, Sutherland GR, Callen DF, Hopwood JJ, Morris CP. 1993. The morquio Asyndrome (mucopolysaccharidosis IVA) gene maps to 16q24.3. Am J Hum Genet 52:96-98.
5. Bas A, Forsberg G, Hammarstrom S, Hammarstrom ML. 2004. Utility of the housekeeping genes 18S rRNA, beta-actin and glyceraldehyde-3-phosphate-dehydrogenase for normalization in real-time quantitative reverse transcriptase-polymerase chain reaction analysis of gene expression in human Tlymphocytes. Scand J Immunol 59:566-573.
6. Batzer MA, Deininger PL. 2002. Alu repeats and human genomic diversity. Nat Rev Genet 3:370-379.
7. Caciotti A, Donati MA, Bardelli T, d'Azzo A, Massai G, Luciani L, Zammarchi E, Morrone A. 2005. Primary and secondary elastin-binding protein defect leads to impaired elastogenesis in fibroblasts from GM1-gangliosidosis patients. Am J Pathol 167:1689-1698.
8. Caciotti A, Garman SC, Rivera-Colon Y, Procopio E, Catarzi S, Ferri L, Guido C, Martelli P, Parini R, Antuzzi D, Battini R, Sibilio M, et al. 2011. GM1 gangliosidosis and Morquio Bdisease: an update on genetic alterations and clinical findings. Biochim Biophys Acta 1812:782-790.
9. Cahill D, Connor B, Carney JP. 2006. Mechanisms of eukaryotic DNAdouble strand break repair. Front Biosci 11:1958-1976.
10. Camelier MV, Burin MG, De Mari J, Vieira TA, Marasca G, Giugliani R. 2011. Practical and reliable enzyme test for the detection of mucopolysaccharidosis IVA(Morquio syndrome type A) in dried blood samples. Clin Chim Acta 412:1805-1808.
11. Carraresi L, Parini R, Filoni C, Caciotti A, Sersale G, Tomatsu S, Orlando C, Zammarchi E, Guerrini R, Donati MA, Morrone A. 2008. GALNSgene expression profiling in Morquio Apatients' fibroblasts. Clin Chim Acta 397:72-76.
12. Cheng J, Randall A, Baldi P. 2006. Prediction of protein stability changes for single-site mutations using support vector machines. Proteins 62:1125-1132.
13. Cooper DN, Bacolla A, Ferec C, Vasquez KM, Kehrer-Sawatzki H, Chen JM. 2011. On the sequence-directed nature of human gene mutation: the role of genomic architecture and the local DNAsequence environment in mediating gene mutations underlying human inherited disease. Hum Mutat 32:1075-1099.
14. Davison JE, Kearney S, Horton J, Foster K, Peet AC, Hendriksz CJ. 2013. Intellectual and neurological functioning in Morquio syndrome (MPSIVA). J Inherit Metab Dis 36:323-328.
15. den Dunnen JT, Antonarakis SE. 2001. Nomenclature for the description of human sequence variations. Hum Genet 109:121-124.
16. Dung VC, Tomatsu S, Montano AM, Gottesman G, Bober MB, Mackenzie W, Maeda M, Mitchell GA, Suzuki Y, Orii T. 2013. Mucopolysaccharidosis IVA: correlation between genotype, phenotype and keratan sulfate levels. Mol Genet Metab 110:129-138.
17. Dvorak-Ewell M, Wendt D, Hague C, Christianson T, Koppaka V, Crippen D, Kakkis E, Vellard M. 2010. Enzyme replacement in a human model of mucopolysaccharidosis IVA in vitro and its biodistribution in the cartilage of wild type mice. PLoS One 5(8):e12194.
18. Ferri L, Funghini S, Fioravanti A, Biondi E, la Marca G, Guerrini R, Donati M, Morrone A. 2014. Aminoacylase I deficiency due to ACY1 mRNAexon skipping. Clin Genet 86:367-372.
19. Firth HV, Richards SM, Bevan AP, Clayton S, Corpas M, Rajan D, Van Vooren S, Moreau Y, Pettett RM, Carter NP. 2009. DECIPHER: Database of Chromosomal Imbalance and Phenotype in Humans Using Ensembl Resources. Am J Hum Genet 84:524-533.
20. Fukuda S, Tomatsu S, Masuno M, Ogawa T, Yamagishi A, Rezvi GM, Sukegawa K, Shimozawa N, Suzuki Y, Kondo N, Imaizumi K, Kuroki Y, et al. 1996. Mucopolysaccharidosis IVA: submicroscopic deletion of 16q24.3 and a novel R386Cmutation of N-acetylgalactosamine-6-sulfate sulfatase gene in a classical Morquio disease. Hum Mutat 7:123-134.
21. Galjaard H. 1980. Genetic metabolic diseases early diagnosis and prenatal analysis. Amsterdam, The Netherlands: Elsevier/North Holland Biochemical Press. p 825.
22. Gu W, Zhang F, Lupski JR. 2008. Mechanisms for human genomic rearrangements. Pathogenetics 1:4.
23. Harmatz P, Mengel KE, Giugliani R, Valayannopoulos V, Lin SP, Parini R, Guffon N, Burton BK, Hendriksz CJ, Mitchell J, Martins A, Jones S, et al. 2013. The Morquio Aclinical assessment program: baseline results illustrating progressive, multisystemic clinical impairments in Morquio Asubjects. Mol Genet Metab 109:54-61.
24. Hendriksz CJ, Burton B, Fleming TR, Harmatz P, Hughes D, Jones SA, Lin SP, Mengel E, Scarpa M, Valayannopoulos V, Giugliani R; STRIVE Investigators, et al. 2014. Efficacy and safety of enzyme replacement therapy with BMN110 (elosulfase alfa) for Morquio Asyndrome (mucopolysaccharidosis IVA): a phase 3 randomised placebo-controlled study. J Inherit Metab Dis 37:979-990.
25. Hendriksz CJ, Harmatz P, Beck M, Jones S, Wood T, Lachman R, Gravance CG, Orii T, Tomatsu S. 2013. Review of clinical presentation and diagnosis of mucopolysaccharidosis IVA. Mol Genet Metab 110:54-64.
26. Hinek A, Smith AC, Cutiongco EM, Callahan JW, Gripp KW, Weksberg R. 2000. Decreased elastin deposition and high proliferation of fibroblasts from Costello syndrome are related to functional deficiency in the 67-kD elastin-binding protein. Am J Hum Genet 66:859-872.
27. Hinek A, Wilson SE. 2000. Impaired elastogenesis in Hurler disease: dermatan sulfate accumulation linked to deficiency in elastin-binding protein and elastic fiber assembly. Am J Pathol 156:925-938.
28. Hori T, Tomatsu S, Nakashima Y, Uchiyama A, Fukuda S, Sukegawa K, Shimozawa N, Suzuki Y, Kondo N, Horiuchi T, Ogura S, Orii T. 1995. Mucopolysaccharidosis type IVA: common double deletion in the N-acetylgalactosamine-6-sulfatase gene (GALNS). Genomics 26:535-542.
29. Joosten RP, te Beek TA, Krieger E, Hekkelman ML, Hooft RW, Schneider R, Sander C, Vriend G. 2011. A series of PDBrelated databases for everyday needs. Nucleic Acids Res 39(Database Issue):D411-D419.
30. Kabsch W, Sander C. 1983. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22:2577-2637.
31. Kent WJ, Sugnet CW, Furey TS, Roskin KM, Pringle TH, Zahler AM, Haussler D. 2002. The human genome browser at UCSC. Genome Res 12:996-1006.
32. Khaliq T, Sadilek M, Scott CR, Turecek F, Gelb MH. 2011. Tandem mass spectrometry for the direct assay of lysosomal enzymes in dried blood spots: application to screening newborns for mucopolysaccharidosis IVA. Clin Chem 57:128-131.
33. Livak KJ, Schmittgen TD. 2001. Analysis of relative gene expression data using real-time quantitative PCRand the 2(-Delta Delta C(T)) Method. Methods 25:402-408.
34. Malvagia S, Morrone A, Caciotti A, Bardelli T, d'Azzo A, Ancora G, Zammarchi E, Donati MA. 2004. New mutations in the PPBGgene lead to loss of PPCAprotein which affects the level of the beta-galactosidase/neuraminidase complex and the EBP-receptor. Mol Genet Metab 82:48-55.
35. Masue M, Sukegawa K, Orii T, Hashimoto T. 1991. N-acetylgalactosamine-6-sulfate sulfatase in human placenta: purification and characteristics. J Biochem 110:965-970.
36. Masuno M, Tomatsu S, Nakashima Y, Hori T, Fukuda S, Masue M, Sukegawa K, Orii T. 1993. Mucopolysaccharidosis IV A: assignment of the human N-acetylgalactosamine-6-sulfate sulfatase (GALNS) gene to chromosome 16q24. Genomics 16:777-778.
37. Matalon R, Arbogast B, Justice P, Brandt IK, Dorfman A. 1974. Morquio's syndrome: deficiency of a chondroitin sulfate N-acetylhexosamine sulfate sulfatase. Biochem Biophys Res Commun 61:759-765.
38. Montano AM, Tomatsu S, Brusius A, Smith M, Orii T. 2008. Growth charts for patients affected with Morquio Adisease. Am J Med Genet A 146A:1286-1295.
39. Montano AM, Tomatsu S, Gottesman GS, Smith M, Orii T. 2007. International Morquio ARegistry: clinical manifestation and natural course of Morquio Adisease. J Inherit Metab Dis 30:165-174.
40. Morrone A, Caciotti A, Atwood R, Davidson K, Du C, Francis-Lyon P, Harmatz P, Mealiffe M, Mooney S, Oron TR, Ryles A, Zawadzki KA, et al. 2014a. Morquio Asyndrome-associated mutations: a review of alterations in the GALNSgene and a new locus-specific database. Human Mutation 35:1271-1279.
41. Morrone A, Tylee KL, Al-Sayed M, Brusius-Facchin AC, Caciotti A, Church HJ, Coll MJ, Davidson K, Fietz MJ, Gort L, Hegde M, Kubaski F, et al. 2014b. Molecular testing of 163 patients with Morquio A(Mucopolysaccharidosis IVA) identifies 39 novel GALNSmutations. Mol Genet Metab 112:160-170.
42. Nakashima Y, Tomatsu S, Hori T, Fukuda S, Sukegawa K, Kondo N, Suzuki Y, Shimozawa N, Orii T. 1994. Mucopolysaccharidosis IV A: molecular cloning of the human N-acetylgalactosamine-6-sulfatase gene (GALNS) and analysis of the 5′-flanking region. Genomics 20:99-104.
43. Nelson J. 1997. Incidence of the mucopolysaccharidoses in Northern Ireland. Hum Genet 101:355-358.
44. Nelson J, Crowhurst J, Carey B, Greed L. 2003. Incidence of the mucopolysaccharidoses in Western Australia. Am J Med Genet A 123A:310-313.
45. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE. 2004. UCSFchimera-a visualization system for exploratory research and analysis. J Comput Chem 25:1605-1612.
46. Rivera-Colon Y, Schutsky EK, Kita AZ, Garman SC. 2012. The structure of human GALNSreveals the molecular basis for mucopolysaccharidosis IV A. J Mol Biol 423:736-751.
47. Stenson PD, Mort M, Ball EV, Howells K, Phillips AD, Thomas NS, Cooper DN. 2009. The Human Gene Mutation Database: 2008 update. Genome Med 1:13.
48. Sukegawa K, Nakamura H, Kato Z, Tomatsu S, Montano AM, Fukao T, Toietta G, Tortora P, Orii T, Kondo N. 2000. Biochemical and structural analysis of missense mutations in N-acetylgalactosamine-6-sulfate sulfatase causing mucopolysaccharidosis IVAphenotypes. Hum Mol Genet 9:1283-1290.
49. Tomatsu S, Filocamo M, Orii KO, Sly WS, Gutierrez MA, Nishioka T, Serrato OP, Di Natale P, Montano AM, Yamaguchi S, Kondo N, Orii T, Noguchi A. 2004. Mucopolysaccharidosis IVA(Morquio A): identification of novel common mutations in the N-acetylgalactosamine-6-sulfate sulfatase (GALNS) gene in Italian patients. Hum Mutat 24:187-188.
50. Tomatsu S, Fujii T, Fukushi M, Oguma T, Shimada T, Maeda M, Kida K, Shibata Y, Futatsumori H, Montano AM, Mason RW, Yamaguchi S, et al. 2013. Newborn screening and diagnosis of mucopolysaccharidoses. Mol Genet Metab 110:42-53.
51. Tomatsu S, Montano AM, Dung VC, Ohashi A, Oikawa H, Oguma T, Orii T, Barrera L, Sly WS. 2010. Enhancement of drug delivery: enzyme-replacement therapy for murine Morquio A syndrome. Mol Ther 18(6):1094-1102.
52. Tomatsu S, Montano AM, Nishioka T, Gutierrez MA, Pena OM, Tranda Firescu GG, Lopez P, Yamaguchi S, Noguchi A, Orii T. 2005. Mutation and polymorphism spectrum of the GALNSgene in mucopolysaccharidosis IVA(Morquio A). Hum Mutat 26:500-512.
53. Tomatsu S, Montano AM, Oikawa H, Smith M, Barrera L, Chinen Y, Thacker MM, Mackenzie WG, Suzuki Y, Orii T. 2011. Mucopolysaccharidosis type IVA(Morquio Adisease): clinical review and current treatment. Curr Pharm Biotechnol 12:931-945.
54. van Diggelen OP, Zhao H, Kleijer WJ, Janse HC, Poorthuis BJ, van Pelt J, Kamerling JP, Galjaard H. 1990. A fluorimetric enzyme assay for the diagnosis of Morquio disease type A(MPSIV A). Clin Chim Acta 187:131-139.
55. Vihinen M. 2013. Guidelines for reporting and using prediction tools for genetic variation analysis. Hum Mutat 34:275-282.
56. Wang L, Ou X, Sebesta I, Vondrak K, Krijt J, Elleder M, Poupetova H, Ledvinova J, Zeman J, Simmonds HA, Tischfield JA, Sahota A. 1999. Combined adenine phosphoribosyltransferase and N-acetylgalactosamine-6-sulfate sulfatase deficiency. Mol Genet Metab 68:78-85.
57. Ward KJ, Ellard S, Yajnik CS, Frayling TM, Hattersley AT, Venigalla PN, Chandak GR. 2006. Allelic drop-out may occur with a primer binding site polymorphism for the commonly used RFLPassay for the -1131T>Cpolymorphism of the Apolipoprotein AVgene. Lipids Health Dis 5:11.
58. Whitley CB, Ridnour MD, Draper KA, Dutton CM, Neglia JP. 1989. Diagnostic test for mucopolysaccharidosis. I. Direct method for quantifying excessive urinary glycosaminoglycan excretion. Clin Chem 35:374-379.
59. Wood TC, Harvey K, Beck M, Burin MG, Chien YH, Church HJ, D'Almeida V, van Diggelen OP, Fietz M, Giugliani R, Harmatz P, Hawley P, et al. 2013. Diagnosing mucopolysaccharidosis IVA. J Inherit Metab Dis 36:293-307.