Fol. Biol. 2017, 63, 165-173

https://doi.org/10.14712/fb2017063050165

Molecular Diagnostics of Copper-Transporting Protein Mutations Allows Early Onset Individual Therapy of Menkes Disease

L. Králík1, E. Flachsová1, H. Hansíková1, V. Saudek2, J. Zeman1, Pavel Martásek1

1Department of Paediatrics and Adolescent Medicine, First Faculty of Medicine, Charles University in Prague and General University Hospital in Prague, Czech Republic
2Wellcome Trust-MRC Institute of Metabolic Science, University of Cambridge Metabolic Research Laboratories, Cambridge, United Kingdom

Received October 2017
Accepted January 2018

References

1. Allen, G. S., Wu, C. C., Cardozo, T., Stokes, D. L. (2011) The architecture of CopA from Archeaoglobus fulgidus studied by cryo-electron microscopy and computational docking. Structure 19, 1219-1232. <https://doi.org/10.1016/j.str.2011.05.014>
2. Andersson, M., Mattle, D., Sitsel, O., Klymchuk, T., Nielsen, A. M., Moller, L. B., White, S. H., Nissen, P., Gourdon, P. (2014) Copper-transporting P-type ATPases use a unique ion-release pathway. Nat. Struct. Mol. Biol. 21, 43-48. <https://doi.org/10.1038/nsmb.2721>
3. Armougom, F., Moretti, S, Poirot O., Audic, S., Dumas, P., Schaeli, B., Keduas, V., Notredame, C. (2006) Expresso: automatic incorporation of structural information in multiple sequence alignments using 3D-Coffee. Nucleic Acids Res. 34, W604-608. <https://doi.org/10.1093/nar/gkl092>
4. Camakaris, J., Voskoboinik, I., Mercer, J. F. (1999) Molecular mechanisms of copper homeostasis. Biochem. Biophys. Res. Commun. 261, 225-232. <https://doi.org/10.1006/bbrc.1999.1073>
5. Chelly, J., Tumer, Z., Tonnesen, T., Petterson, A., Ishikawa- Brush, Y., Tommerup, N., Horn, N., Monaco, A. P. (1993) Isolation of a candidate gene for Menkes disease that encodes a potential heavy metal binding protein. Nat. Genet. 3, 14-19. <https://doi.org/10.1038/ng0193-14>
6. Daish, P., Wheeler, E. M., Roberts, P. F., Jones, R. D. (1978) Menkes’s syndrome. Report of a patient treated from 21 days of age with parenteral copper. Arch. Dis. Child. 53, 956-958. <https://doi.org/10.1136/adc.53.12.956>
7. Das, S., Levinson, B., Vulpe, C., Whitney, S., Gitschier, J., Packman, S. (1995) Similar splicing mutations of the Menkes/ mottled copper-transporting ATPase gene in occipital horn syndrome and the blotchy mouse. Am. J. Hum. Genet. 56, 570-576.
8. DiMauro, S., Lombes, A., Nakase, H., Mita, S., Fabrizi, G. M., Tritschler, H. J., Bonilla, E., Miranda, A. F., DeVivo, D. C., Schon, E. A. (1990) Cytochrome c oxidase deficiency. Pediatr. Res. 28, 536-541. <https://doi.org/10.1203/00006450-199011000-00025>
9. Fox, J. E., Reynolds, C. C., Boyles, J. K. (1992) Studying the platelet cytoskeleton in Triton X-100 lysates. Meth. Enzymol. 215, 42-58. <https://doi.org/10.1016/0076-6879(92)15052-E>
10. Grover, W. D., Scrutton, M. C. (1975) Copper infusion therapy in trichopoliodystrophy. J. Pediatr. 86, 216-220. <https://doi.org/10.1016/S0022-3476(75)80471-9>
11. Haddad, M. R., Macri, C. J., Holmes, C. S., Goldstein, D. S., Jacobson, B. E., Centeno, J. A., Popek, E. J., Gahl, W. A, Kaler, S. G. 2012. In utero copper treatment for Menkes disease associated with a severe ATP7A mutation. Mol. Genet. Metab. 107, 222-228. <https://doi.org/10.1016/j.ymgme.2012.05.008>
12. Hahn, S., Cho, K., Ryu, K., Kim, J., Pai, K., Kim, M., Park, H., Yoo, O. (2001) Identification of four novel mutations in classical Menkes disease and successful prenatal DNA diagnosis. Mol. Genet. Metab. 73, 86-90. <https://doi.org/10.1006/mgme.2001.3169>
13. Hamza, I., Faisst, A., Prohaska, J., Chen, J., Gruss, P., Gitlin, J. D. (2001) The metallochaperone Atox1 plays a critical role in perinatal copper homeostasis. Proc. Natl. Acad. Sci. USA 98, 6848-6852. <https://doi.org/10.1073/pnas.111058498>
14. Kaler, S. G., Gallo, L. K., Proud, V. K., Percy, A. K., Mark, Y., Segal, N. A., Goldstein, D. S., Holmes, C. S., Gahl, W. A. (1994) Occipital horn syndrome and a mild Menkes phenotype associated with splice site mutations at the MNK locus. Nat. Genet. 8, 195-202. <https://doi.org/10.1038/ng1094-195>
15. Kaler, S. G. (1998) Diagnosis and therapy of Menkes syndrome, a genetic form of copper deficiency. Am. J. Clin. Nutr. 67, 1029S-1034S. <https://doi.org/10.1093/ajcn/67.5.1029S>
16. Kaler, S. G., Holmes, C. S., Goldstein, D. S., Tang, J., Godwin, S. C., Donsante, A., Liew, C. J., Sato, S., Patronas, N. (2008). Neonatal diagnosis and treatment of Menkes disease. N. Engl. J. Med. 358, 605-614. <https://doi.org/10.1056/NEJMoa070613>
17. Kaler, S. G. (2014) Neurodevelopment and brain growth in classic Menkes disease is influenced by age and symptomatology at initiation of copper treatment. J. Trace Elem. Med. Biol. 28, 427-430. <https://doi.org/10.1016/j.jtemb.2014.08.008>
18. Kennerson, M. L., Nicholson, G. A., Kaler, S. G., Kowalski, B., Mercer, J. F., Tang, J., Llanos, R. M., Chu, S., Takata, R. I., Speck-Martins, C. E., Baets, J., Almeida-Souza, L., Fischer, D., Timmerman, V., Taylor, P. E., Scherer, S. S., Ferguson, T. A., Bird, T. D., De Jonghe, P., Feely, S, M., Shy, M. E., Garbern, J. Y. (2010) Missense mutations in the copper transporter gene ATP7A cause X-linked distal hereditary motor neuropathy. Am. J. Hum. Genet. 86, 343-352. <https://doi.org/10.1016/j.ajhg.2010.01.027>
19. Kodama, H., Murata, Y. (1999) Molecular genetics and pathophysiology of Menkes disease. Pediatr. Int. 41, 430-435. <https://doi.org/10.1046/j.1442-200x.1999.01091.x>
20. Liu, P. C., McAndrew, P. E., Kaler, S. G. (2002) Rapid and robust screening of the Menkes disease/occipital horn syndrome gene. Genet. Test. 6, 255-260. <https://doi.org/10.1089/10906570260471778>
21. Lowry, O. H., Rosebrough, N. J., Farr, A. L., Randall, R. J. (1951) Protein measurement with the Folin phenol reagent. J. Biol. Chem. 193, 265-275. <https://doi.org/10.1016/S0021-9258(19)52451-6>
22. Lutsenko, S., Petris, M. J. (2003) Function and regulation of the mammalian copper-transporting ATPases: insights from biochemical and cell biological approaches. J. Membr. Biol. 191, 1-12. <https://doi.org/10.1007/s00232-002-1040-6>
23. Menkes, J. H., Alter, M., Steigleder, G. K., Weakley, D. R., Sung, J. H. (1962) A sex-linked recessive disorder with retardation of growth, peculiar hair, and focal cerebral and cerebellar degeneration. Pediatrics 29, 764-779.
24. Mercer, J. F., Livingston, J., Hall, B., Paynter, J. A., Begy, C., Chandrasekharappa, S., Lockhart, P., Grimes, A., Bhave, M., Siemieniak, D., et al. (1993) Isolation of a partial candidate gene for Menkes disease by positional cloning. Nat. Genet. 3, 20-25. <https://doi.org/10.1038/ng0193-20>
25. Moore, S. D., Helmle, K. E., Prat, L. M., Cox, D. W. (2002) Tissue localization of the copper chaperone ATOX1 and its potential role in disease. Mamm. Genome 13, 563-568. <https://doi.org/10.1007/s00335-002-2172-9>
26. Petris, M. J., Mercer, J. F., Culvenor, J. G., Lockhart, P., Gleeson, P. A., Camakaris, J. (1996) Ligand-regulated transport of the Menkes copper P-type ATPase efflux pump from the Golgi apparatus to the plasma membrane: a novel mechanism of regulated trafficking. EMBO J. 15, 6084-6095. <https://doi.org/10.1002/j.1460-2075.1996.tb00997.x>
27. Robinson, B. H., MacMillan, H., Petrova-Benedict, R., Sherwood, W. G. (1987) Variable clinical presentation in patients with defective E1 component of pyruvate dehydrogenase complex. J. Pediatr. 111, 525-533. <https://doi.org/10.1016/S0022-3476(87)80112-9>
28. Rustin, P., Chretien, D., Bourgeron, T., Gerard, B., Rotig, A., Saudubray, J. M., Munnich, A. (1994) Biochemical and molecular investigations in respiratory chain deficiencies. Clin. Chim. Acta 228, 35-51. <https://doi.org/10.1016/0009-8981(94)90055-8>
29. Sali, A., Blundell, T. L. (1993) Comparative protein modelling by satisfaction of spatial restraints. J. Mol. Biol, 234, 779-815. <https://doi.org/10.1006/jmbi.1993.1626>
30. Sarkar, B., Lingertat-Walsh, K., Clarke, J. T. (1993) Copperhistidine therapy for Menkes disease. J. Pediatr. 123, 828-830. <https://doi.org/10.1016/S0022-3476(05)80870-4>
31. Simon, I., Schaefer, M., Reichert, J., Stremmel, W. (2008) Analysis of the human Atox 1 homologue in Wilson patients. World J. Gastroenterol. 14, 2383-2387. <https://doi.org/10.3748/wjg.14.2383>
32. Srere, P. A. (1969) Citrate synthase. In: Methods in Enzymology, pp. 3–11, Elsevier.
33. Tonnesen, T., Kleijer, W. J., Horn, N. (1991) Incidence of Menkes disease. Hum. Genet. 86, 408-410. <https://doi.org/10.1007/BF00201846>
34. Tumer, Z., Vural, B., Tonnesen, T., Chelly, J., Monaco, A. P., Horn, N. (1995) Characterization of the exon structure of the Menkes disease gene using vectorette PCR. Genomics 26, 437-442. <https://doi.org/10.1016/0888-7543(95)80160-N>
35. Tumer, Z., Lund, C., Tolshave, J., Vura,l B., Tonnesen, T., Horn, N. (1997) Identification of point mutations in 41 unrelated patients affected with Menkes disease. Am. J. Hum. Genet. 60, 63-71.
36. Tumer, Z., Birk Moller, L., Horn N. (2003) Screening of 383 unrelated patients affected with Menkes disease and finding of 57 gross deletions in ATP7A. Hum. Mutat. 22, 457-464. <https://doi.org/10.1002/humu.10287>
37. Vulpe, C., Levinson, B., Whitney, S., Packman, S., Gitschier, J. (1993) Isolation of a candidate gene for Menkes disease and evidence that it encodes a copper-transporting ATPase. Nat Genet 3, 7-13. <https://doi.org/10.1038/ng0193-7>
38. Yamaguchi, Y., Heiny, M. E., Gitlin, J. D. (1993) Isolation and characterization of a human liver cDNA as a candidate gene for Wilson disease. Biochem. Biophys. Res. Commun. 197, 271-277. <https://doi.org/10.1006/bbrc.1993.2471>
39. Yi, L., Kaler S. G. (2015) Direct interactions of adaptor protein complexes 1 and 2 with the copper transporter ATP7A mediate its anterograde and retrograde trafficking. Hum. Mol. Genet. 24, 2411-2425. <https://doi.org/10.1093/hmg/ddv002>
front cover

ISSN 0015-5500 (Print) ISSN 2533-7602 (Online)

Open access journal

Archive