Fol. Biol. 2016, 62, 82-89

https://doi.org/10.14712/fb2016062020082

X-Chromosome Inactivation Analysis in Different Cell Types and Induced Pluripotent Stem Cells Elucidates the Disease Mechanism in a Rare Case of Mucopolysaccharidosis Type II in a Female

M. Řeboun1, J. Rybová1, R. Dobrovolný1, J. Včelák2, T. Veselková1, G. Štorkánová1, D. Mušálková1, M. Hřebíček1, J. Ledvinová1, M. Magner3, J. Zeman3, K. Pešková1, Lenka Dvořáková1

1Institute of Inherited Metabolic Disorders, First Faculty of Medicine, Charles University in Prague and General University Hospital in Prague, Czech Republic
2Institute of Endocrinology, Prague, Czech Republic
3Department of Paediatrics and Adolescent Medicine, First Faculty of Medicine, Charles University in Prague and General University Hospital in Prague, Czech Republic

Received December 2015
Accepted February 2016

References

1. Bhatnagar, S., Zhu, X., Ou, J., Lin, L., Chamberlain, L., Zhu, L. J., Wajapeyee, N., Green, M. R. (2014) Genetic and pharmacological reactivation of the mammalian inactive X chromosome. Proc. Natl. Acad. Sci. USA 111, 12591-12598. <https://doi.org/10.1073/pnas.1413620111>
2. Briggs, S. F., Reijo Pera, R. A. (2014) X chromosome inactivation: recent advances and a look forward. Curr. Opin. Genet. Dev. 28, 78-82. <https://doi.org/10.1016/j.gde.2014.09.010>
3. Brusius-Facchin, A. C., Schwartz, I. V., Zimmer, C., Ribeiro, M. G., Acosta, A. X., Horovitz, D., Monlleo, I. L., Fontes, M. I., Fett-Conte, A., Sobrinho, R. P., Duarte, A. R., Boy, R., Mabe, P., Ascurra, M., de Michelena, M., Tylee, K. L., Besley, G. T., Garreton, M. C., Giugliani, R., Leistner- Segal, S. (2014) Mucopolysaccharidosis type II: identification of 30 novel mutations among Latin American patients. Mol. Genet. Metab. 111, 133-138. <https://doi.org/10.1016/j.ymgme.2013.08.011>
4. Conzelmann, E., Sandhoff, K. (1983) Partial enzyme deficiencies: residual activities and the development of neurological disorders. Dev. Neurosci. 6, 58-71. <https://doi.org/10.1159/000112332>
5. Cotton, A. M., Ge, B., Light, N., Adoue, V., Pastinen, T., Brown, C. J. (2013) Analysis of expressed SNPs identifies variable extents of expression from the human inactive X chromosome. Genome Biol. 14, R122. <https://doi.org/10.1186/gb-2013-14-11-r122>
6. Echevarria, L., Benistan, K., Toussaint, A., Dubourg, O., Hagege, A. A., Eladari, D., Jabbour, F., Beldjord, C., De Mazancourt, P., Germain, D. P. (2016) X-chromosome inactivation in female patients with Fabry disease. Clin. Genet. 89, 44-54. <https://doi.org/10.1111/cge.12613>
7. Fuller, M., Mellett, N., Hein, L. K., Brooks, D. A., Meikle, P. J. (2015) Absence of α-galactosidase cross-correction in Fabry heterozygote cultured skin fibroblasts. Mol. Genet. Metab. 114, 268-273. <https://doi.org/10.1016/j.ymgme.2014.11.005>
8. Gafni, O., Weinberger, L., Mansour, A. A., Manor, Y. S., Chomsky, E., Ben-Yosef, D., Kalma, Y., Viukov, S., Maza, I., Zviran, A., Rais, Y., Shipony, Z., Mukamel, Z., Krupalnik, V., Zerbib, M., Geula, S., Caspi, I., Schneir, D., Shwartz, T., Gilad, S., Amann-Zalcenstein, D., Benjamin, S., Amit, I., Tanay, A., Massarwa, R., Novershtern, N., Hanna, J. H. (2013) Derivation of novel human ground state naive pluripotent stem cells. Nature 504, 282-286. <https://doi.org/10.1038/nature12745>
9. Hartree, E. F. (1972) Determination of protein: a modification of the Lowry method that gives a linear photometric response. Anal. Biochem. 48, 422-427. <https://doi.org/10.1016/0003-2697(72)90094-2>
10. Jurecka, A., Krumina, Z., Zuber, Z., Rozdzynska-Swiatkowska, A., Kloska, A., Czartoryska, B., Tylki-Szymanska, A. (2012) Mucopolysaccharidosis type II in females and response to enzyme replacement therapy. Am. J. Med. Genet. A 158A, 450-454. <https://doi.org/10.1002/ajmg.a.34415>
11. Kim, D., Pertea, G., Trapnell, C., Pimentel, H., Kelley, R., Salzberg, S. L. (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol. 14, R36. <https://doi.org/10.1186/gb-2013-14-4-r36>
12. Lian, X., Zhang, J., Azarin, S. M., Zhu, K., Hazeltine, L. B., Bao, X., Hsiao, C., Kamp, T. J., Palecek, S. P. (2013) Directed cardiomyocyte differentiation from human pluripotent stem cells by modulating Wnt/β-catenin signaling under fully defined conditions. Nat. Protoc. 8, 162-175. <https://doi.org/10.1038/nprot.2012.150>
13. Lonardo, F., Di Natale, P., Lualdi, S., Acquaviva, F., Cuoco, C., Scarano, F., Maioli, M., Pavone, L. M., Di Gregorio, G., Filocamo, M., Scarano, G. (2014) Mucopolysaccharidosis type II in a female patient with a reciprocal X;9 translocation and skewed X chromosome inactivation. Am. J. Med. Genet. A 164A, 2627-2632. <https://doi.org/10.1002/ajmg.a.36667>
14. Lopez-Marin, L., Gutierrez-Solana, L. G., Azuara, L. A., de Las Heras, R. S., Rodriguez, A. D., Extremera, V. C. (2013) Detection by urinary GAG testing of mucopolysaccharidosis type II in an at-risk Spanish population. JIMD Rep. 10, 61-68. <https://doi.org/10.1007/8904_2012_204>
15. Mossner, M., Nolte, F., Hutter, G., Reins, J., Klaumunzer, M., Nowak, V., Oblander, J., Ackermann, K., Will, S., Rohl, H., Neumann, U., Neumann, M., Hopfer, O., Baldus, C. D., Hofmann, W. K., Nowak, D. (2013) Skewed X-inactivation patterns in ageing healthy and myelodysplastic haematopoiesis determined by a pyrosequencing based transcriptional clonality assay. J. Med. Genet. 50, 108-117. <https://doi.org/10.1136/jmedgenet-2012-101093>
16. Muenzer, J., Hendriksz, C. J., Fan, Z., Vijayaraghavan, S., Perry, V., Santra, S., Solanki, G. A., Mascelli, M. A., Pan, L., Wang, N., Sciarappa, K., Barbier, A. J. (2016) A phase I/II study of intrathecal idursulfase-IT in children with severe mucopolysaccharidosis II. Genet. Med. 18, 73-81. <https://doi.org/10.1038/gim.2015.36>
17. Musalkova, D., Minks, J., Storkanova, G., Dvorakova, L., Hrebicek, M. (2015) Identification of novel informative loci for DNA-based X-inactivation analysis. Blood Cells Mol. Dis. 54, 210-216. <https://doi.org/10.1016/j.bcmd.2014.10.001>
18. Neufeld, E. F., Muenzer, J. (2001) The mucopolysaccharidoses. In: The Metabolic and Molecular Bases of Inherited Disease, eds. Scriver, C. R., Beaudet, A. L., Sly, W. S., Valle, D., pp. 3421-3452, McGraw-Hill Co., New York
19. Pina-Aguilar, R. E., Zaragoza-Arevalo, G. R., Rau, I., Gal, A., Alcantara-Ortigoza, M. A., Lopez-Martinez, M. S., Santillan-Hernandez, Y. (2013) Mucopolysaccharidosis type II in a female carrying a heterozygous stop mutation of the iduronate-2-sulfatase gene and showing a skewed X chromosome inactivation. Eur. J. Med. Genet. 56, 159-162. <https://doi.org/10.1016/j.ejmg.2012.11.006>
20. Poupetova, H., Ledvinova, J., Berna, L., Dvorakova, L., Kozich, V., Elleder, M. (2010) The birth prevalence of lysosomal storage disorders in the Czech Republic: comparison with data in different populations. J. Inherit. Metab. Dis. 33, 387-396. <https://doi.org/10.1007/s10545-010-9093-7>
21. Racchi, O., Mangerini, R., Rapezzi, D., Rolfo, M., Gaetani, G. F., Ferraris, A. M. (1998) X chromosome inactivation patterns in normal females. Blood Cells Mol. Dis. 24, 439-447. <https://doi.org/10.1006/bcmd.1998.0213>
22. Scarpa, M., Almassy, Z., Beck, M., Bodamer, O., Bruce, I. A., De Meirleir, L., Guffon, N., Guillen-Navarro, E., Hensman, P., Jones, S., Kamin, W., Kampmann, C., Lampe, C., Lavery, C. A., Teles, E. L., Link, B., Lund, A. M., Malm, G., Pitz, S., Rothera, M., Stewart, C., Tylki-Szymanska, A., van der Ploeg, A., Walker, R., Zeman, J., Wraith, J. E., Hunter Syndrome European Expert Council (2011) Mucopolysaccharidosis type II: European recommendations for the diagnosis and multidisciplinary management of a rare disease. Orphanet J. Rare Dis. 6, 72. <https://doi.org/10.1186/1750-1172-6-72>
23. Skoog, W. A., Beck, W. S. (1956) Studies on the fibrinogen, dextran and phytohemagglutinin methods of isolating leukocytes. Blood 11, 436-454. <https://doi.org/10.1182/blood.V11.5.436.436>
24. Stacpoole, S. R., Bilican, B., Webber, D. J., Luzhynskaya, A., He, X. L., Compston, A., Karadottir, R., Franklin, R. J., Chandran, S. (2011) Efficient derivation of NPCs, spinal motor neurons and midbrain dopaminergic neurons from hESCs at 3% oxygen. Nat. Protoc. 6, 1229-1240. <https://doi.org/10.1038/nprot.2011.380>
25. Swierczek, S. I., Piterkova, L., Jelinek, J., Agarwal, N., Hammoud, S., Wilson, A., Hickman, K., Parker, C. J., Cairns, B. R., Prchal, J. T. (2012) Methylation of AR locus does not always reflect X chromosome inactivation state. Blood 119, e100-109. <https://doi.org/10.1182/blood-2011-11-390351>
26. Tajima, G., Sakura, N., Kosuga, M., Okuyama, T., Kobayashi, M. (2013) Effects of idursulfase enzyme replacement therapy for mucopolysaccharidosis type II when started in early infancy: comparison in two siblings. Mol. Genet. Metab. 108, 172-177. <https://doi.org/10.1016/j.ymgme.2012.12.010>
27. Tuschl, K., Gal, A., Paschke, E., Kircher, S., Bodamer, O. A. (2005) Mucopolysaccharidosis type II in females: case report and review of literature. Pediatr. Neurol. 32, 270-272. <https://doi.org/10.1016/j.pediatrneurol.2004.10.009>
28. Tylki-Szymanska, A., Jurecka, A., Zuber, Z., Rozdzynska, A., Marucha, J., Czartoryska, B. (2012) Enzyme replacement therapy for mucopolysaccharidosis II from 3 months of age: a 3-year follow-up. Acta Paediatr. 101, e42-47. <https://doi.org/10.1111/j.1651-2227.2011.02385.x>
29. Voznyi, Y. V., Keulemans, J. L., van Diggelen, O. P. (2001) A fluorimetric enzyme assay for the diagnosis of MPS II (Hunter disease). J. Inherit. Metab. Dis. 24, 675-680. <https://doi.org/10.1023/A:1012763026526>
30. Wakabayashi, T., Shimada, Y., Akiyama, K., Higuchi, T., Fukuda, T., Kobayashi, H., Eto, Y., Ida, H., Ohashi, T. (2015) Hematopoietic stem cell gene therapy corrects neuropathic phenotype in murine model of mucopolysaccharidosis type II. Hum. Gene Ther. 26, 357-366. <https://doi.org/10.1089/hum.2014.158>
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