Cutis laxa, exocrine pancreatic insufficiency and altered cellular metabolomics as additional symptoms in a new patient with ATP6AP1-CDG

Molecular Genetics and Metabolism

Volumn 123, Issue 3, 2018, Pages 364-374

  Dimitrov, Bianca ^a   Himmelreich, Nastassja ^a   Hipgrave Ederveen, Agnes L ^b   Lüchtenborg, Christian ^c   Okun, Jürgen G ^a   Breuer, Maximilian ^a   Hutter, Anna Marlen ^a   Carl, Matthias ^c,h   Guglielmi, Luca ^c,h   Hellwig, Andrea ^c   Thiemann, Kai Christian ^a   Jost, Markus ^a   Peters, Verena ^a   Staufner, Christian ^a   Hoffmann, Georg F ^a   Hackenberg, Annette ^d   Paramasivam, Nagarajan ^e,f   Wiemann, Stefan ^f   Eils, Roland ^c,f   Schlesner, Matthias ^f   Strahl, Sabine ^c   Brügger, Britta ^c   Wuhrer, Manfred ^b   Christoph Korenke, G ^g   Thiel, Christian ^a   more..

^a Center for Pediatrics and Adolescent Medicine   (Germany)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d UNIVERSITY CHILDREN S HOSPITAL   (Switzerland)

^e UNIVERSITY OF HEIDELBERG   (Germany)

^f GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^g UNIVERSITY OF OLDENBURG   (Germany)

^h UNIVERSITY OF TRENTO   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLCARNITINE; ADENOSINE TRIPHOSPHATASE; ATP6AP1 PROTEIN; CATALASE; CERAMIDE; CHOLESTEROL; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLETHANOLAMINE; UNCLASSIFIED DRUG; ACOX3 PROTEIN, HUMAN; ACYL COENZYME A OXIDASE; ATP6AP1 PROTEIN, HUMAN; CAT PROTEIN, HUMAN; FATTY ACID; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE;

ARTICLE; CELL PROLIFERATION; CONGENITAL DISORDER OF GLYCOSYLATION; CUTIS LAXA; ENZYME ACTIVITY; EXOCRINE PANCREATIC INSUFFICIENCY; FIBROBLAST; GENE MUTATION; HEPATOSPLENOMEGALY; HUMAN; HUMAN CELL; METABOLOMICS; PEROXISOME; PRIORITY JOURNAL; PROTEIN EXPRESSION; WHOLE EXOME SEQUENCING; CASE REPORT; DEFICIENCY; GENETICS; INFANT; MALE; METABOLISM; METABOLOME; OXIDATION REDUCTION REACTION; X CHROMOSOMAL INHERITANCE;

ACYL-COA OXIDASE; CATALASE; CONGENITAL DISORDERS OF GLYCOSYLATION; CUTIS LAXA; EXOCRINE PANCREATIC INSUFFICIENCY; FATTY ACIDS; GENES, X-LINKED; HUMANS; INFANT; MALE; METABOLOME; METABOLOMICS; OXIDATION-REDUCTION; VACUOLAR PROTON-TRANSLOCATING ATPASES; WHOLE EXOME SEQUENCING;

EID: 85040998042     PISSN: 10967192     EISSN: 10967206     Source Type: Journal    
DOI: 10.1016/j.ymgme.2018.01.008     Document Type: Article

References (46)

1. Madshus, I.H., Regulation of intracellular pH in eukaryotic cells. Biochem. J. 250 (1988), 1–8.
2. Casey, J.R., Grinstein, S., Orlowski, J., Sensors and regulators of intracellular pH. Nat. Rev. Mol. Cell Biol. 11 (2010), 50–61.
3. Marshansky, V., Rubinstein, J.L., Grüber, G., Eukaryotic V-ATPase: novel structural findings and functional insights. Biochim. Biophys. Acta 1837 (2014), 857–879.
4. Finbow, M.E., Harrison, M.A., The vacuolar H +-ATPase: a universal proton pump of eukaryotes. Biochem. J. 324 (1997), 697–712.
5. Cotter, K., Stransky, L., McGuire, C., Forgac, M., Recent insights into the structure, regulation, and function of the V-ATPases. Trends Biochem. Sci. 40 (2015), 611–622.
6. Batlle, D., Haque, S.K., Genetic causes and mechanisms of distal renal tubular acidosis. Nephrol. Dial. Transplant. 27 (2012), 3691–3704.
7. Van Damme, T., Gardeitchik, T., Mohamed, M., Guerrero-Castillo, S., Freisinger, P., Guillemyn, B., Kariminejad, A., Dalloyaux, D., Van Kraaij, S., Lefeber, D.J., Syx, D., Steyaert, W., De Rycke, R., Hoischen, A., Kamsteeg, E.J., Wong, S.Y., Van Scherpenzeel, M., Jamali, P., Brandt, U., Nijtmans, L., Korenke, G.C., Chung, B.H.Y., Mak, C.C.Y., Hausser, I., Kornak, U., Fischer-Zirnsak, B., Strom, T.M., Meitinger, T., Alanay, Y., Utine, G.E., Leung, P.K.C., Ghaderi-Sohi, S., Coucke, P., Symoens, S., De Paepe, A., Thiel, C., Haack, T.B., Malfait, F., Morava, E., Callewaert, B., Wevers, R.A., Mutations in ATP6V1E1 or ATP6V1A cause autosomal-recessive cutis laxa. Am. J. Hum. Genet. 100 (2017), 216–227.
8. Kornak, U., Schulz, A., Friedrich, W., Uhlhaas, S., Kremens, B., Voit, T., Hasan, C., Bode, U., Jentsch, T.J., Kubisch, C., Mutations in the a3 subunit of the vacuolar H(+)-ATPase cause infantile malignant osteopetrosis. Hum. Mol. Genet. 9 (2000), 2059–2063.
9. Frattini, A., Orchard, P.J., Sobacchi, C., Giliani, S., Abinun, M., Mattsson, J.P., Keeling, D.J., Andersson, A.K., Wallbrandt, P., Zecca, L., Notarangelo, L.D., Vezzzoni, P., Villa, A., Defects in TCIRG1 subunit of the vacuolar proton pump are responsible for a subset of human autosomal recessive osteopetrosis. Nat. Genet. 25 (2000), 343–346.
10. Borthwick, K.J., Karet, F.E., Inherited disorders of the H +-ATPase. Curr. Opin. Nephrol. Hypertens. 11 (2002), 563–568.
11. Gupta, H.V., Vengoechea, J., Sahaya, K., Virmani, T., A splice site mutation in ATP6AP2 causes X-linked intellectual disability, epilepsy, and parkinsonism. Parkinsonism Relat. Disord. 21 (2015), 1473–1475.
12. Jaeken, J., Péanne, R., What is new in CDG?. J. Inherit. Metab. Dis. 40 (2017), 569–586.
13. Kornak, U., Reynders, E., Dimopoulou, A., Van Reeuwijk, J., Fischer, B., Rajab, A., Budde, B., Nürnberg, P., Foulquier, F., ARCL Debré-type Study Group, Lefeber, D., Urban, Z., Gruenewald, S., Annaert, W., Brunner, H.G., Van Bokhoven, H., Wevers, R., Morava, E., Matthijs, G., Van Maldergem, L., Mundlos, S., Impaired glycosylation and cutis laxa caused by mutations in the vesicular H +-ATPase subunit ATP6V0A2. Nat. Genet. 40 (2008), 32–34.
14. Jansen, E.J., Timal, S., Ryan, M., Ashikov, A., Van Scherpenzeel, M., Graham, L.A., Mandel, H., Hoischen, A., Iancu, T.C., Raymond, K., Steenbergen, G., Gilissen, C., Huijben, K., Van Bakel, N.H., Maeda, Y., Rodenburg, R.J., Adamowicz, M., Crushell, E., Koenen, H., Adams, D., Vodopiutz, J., Greber-Platzer, S., Müller, T., Dueckers, G., Morava, E., Sykut-Cegielska, J., Martens, G.J., Wevers, R.A., Niehues, T., Huynen, M.A., Veltman, J.A., Stevens, T.H., Lefeber, D.J., ATP6AP1 deficiency causes an immunodeficiency with hepatopathy, cognitive impairment and abnormal protein glycosylation. Nat. Commun., 7, 2016, 11600.
15. Niehues, R., Hasilik, M., Alton, G., Körner, C., Schiebe-Sukumar, M., Koch, H.G., Zimmer, K.P., Wu, R., Harms, E., Reiter, K., Von Figura, K., Freeze, H.H., Harms, H.K., Marquardt, T., Carbohydrate-deficient glycoprotein syndrome type 1b. Phosphomannose isomerase deficiency and mannose therapy. J. Clin. Invest. 101 (1998), 1414–1420.
16. Wopereis, S., Grünewald, S., Morava, E., Penzien, J.M., Briones, P., García-Silva, M.T., Demacker, P.N., Huijben, K.M., Wevers, R.A., Apolipoprotein C-III isofocusing in the diagnosis of genetic defects in O-glycan biosynthesis. Clin. Chem. 49 (2003), 1839–1845.
17. Lübbehusen, J., Thiel, C., Rind, N., Ungar, D., Prinsen, B.H., De Koning, T.J., Van Hasselt, P.M., Körner, C., Fatal outcome due to deficiency of subunit 6 of the conserved oligomeric Golgi complex leading to a new type of congenital disorders of glycosylation. Hum. Mol. Genet. 19 (2010), 3623–3633.
18. Reiding, K.R., Blank, D., Kuijper, D.M., Deelder, A.M., Wuhrer, M., High-throughput profiling of protein N-glycosylation by MALDI-TOF-MS employing linkage-specific sialic acid esterification. Anal. Chem. 86 (2014), 5784–5793.
19. Evers, C., Staufner, C., Granzow, M., Paramasivam, N., Hinderhofer, K., Kaufmann, L., Fischer, C., Thiel, C., Opladen, T., Kotzaeridou, U., Wiemann, S., Schlesner, M., Eils, R., Kölker, S., Bartram, C.R., Hoffmann, G.F., Moog, U., Impact of clinical exomes in neurodevelopmental and neurometabolic disorders. Mol. Genet. Metab. 121 (2017), 297–307.
20. Hansske, B., Thiel, C., Lübke, T., Hasilik, M., Höning, S., Peters, V., Heidemann, P.H., Hoffmann, G.F., Berger, E.G., Von Figura, K., Körner, C., Deficiency of UDP-galactose: N-acetylglucosamine beta-1,4-galactosyltransferase I causes the congenital disorder of glycosylation type II. J. Clin. Invest. 109 (2002), 725–733.
21. Okun, J.G., Conway, S., Schmidt, K.V., Schumacher, J., Wang, X., De Guia, R., Zota, A., Klement, J., Seibert, O., Peters, A., Maida, A., Herzig, S., Rose, A.J., Molecular regulation of urea cycle function by the liver glucocorticoid receptor. Mol. Metab. 4 (2015), 732–740.
22. Ahlgren, H., Bas-Orth, C., Freitag, H.E., Hellwig, A., Ottersen, O.P., Bading, H., The nuclear calcium signaling target, activating transcription factor 3 (ATF3), protects against dendrotoxicity and facilitates the recovery of synaptic transmission after an excitotoxic insult. J. Biol.Chem. 289 (2014), 9970–9982.
23. Özbalci, C., Sachsenheimer, T., Brügger, B., Quantitative analysis of cellular lipids by nano-electrospray ionization mass spectrometry. Methods Mol. Biol. 1033 (2013), 3–20.
24. Hellman, N.E., Gitlin, J.D., Ceruloplasmin: metabolism and function. Annu. Rev. Nutr. 22 (2002), 439–458.
25. Nijhof, W., Holtrop, M., De Jonge, J., Hartsuiker, H., De Vries, H., Severe reductions in transcripts for cytochrome c oxidase during erythropoiesis in vitro do not lead to inactive mitochondria in reticulocytes. Exp. Hematol. 19 (1991), 359–363.
26. Bustos, R.I., Jensen, E.L., Ruiz, L.M., Rivera, S., Ruiz, S., Simon, F., Riedel, C., Ferrick, D., Elorza, A.A., Copper deficiency alters cell bioenergetics and induces mitochondrial fusion through up-regulation of MFN2 and OPA1 in erythropoietic cells. Biochem. Biophys. Res. Commun. 437 (2013), 426–432.
27. Tarasenko, T.N., Pacheco, S.E., Koenig, M.K., Gomez-Rodriguez, J., Kapnick, S.M., Diaz, F., Zerfas, P.M., Barca, E., Sudderth, J., DeBerardinis, R.J., Covian, R., Balaban, R.S., DiMauro, S., McGuire, P.J., Cytochrome c oxidase activity is a metabolic checkpoint that regulates cell fate decisions during T cell activation and differentiation. Cell Metab. 25 (2017), 1254–1268.
28. Smith-Mungo, L.I., Kagan, H.M., Lysyl oxidase: properties, regulation and multiple functions in biology. Matrix Biol. 16 (1998), 387–398.
29. Khakoo, A., Thomas, R., Trompeter, R., Duffy, P., Price, R., Pope, F.M., Congenital cutis laxa and lysyl oxidase deficiency. Clin. Genet. 51 (1997), 109–114.
30. Kodama, H., Fujisawa, C., W. Bhadhprasit Curr Drug Metab, Inherited Copper Transport Disorders: Biochemical Mechanisms, Diagnosis, and Treatment. 13, 2012, 237–250.
31. Urban, Z., Davis, E.C., Cutis laxa: intersection of elastic fiber biogenesis, TGFβ signaling, the secretory pathway and metabolism. Matrix Biol. 33 (2014), 16–22.
32. Hill, V.A., Seymour, C.A., Mortimer, P.S., Pencillamine-induced elastosis perforans serpiginosa and cutis laxa in Wilson's disease. Br. J. Dermatol. 142 (2000), 560–561.
33. Van Maldergem, L., Dobyns, W., Korna, U., ATP6V0A2-Related Cutis Laxa. Pagon, R.A., Adam, M.P., Ardinger, H.H., Wallace, S.E., Amemiya, A., Bean, L.J.H., Bird, T.D., Ledbetter, N., Mefford, H.C., Smith, R.J.H., Stephens, K., (eds.) GeneReviews® [Internet]. Seattle (WA), 2009, University of Washington, Seattle.
34. Mohamed, M., Guillard, M., Wortmann, S.B., Cirak, S., Marklova, E., Michelakakis, H., Korsch, E., Adamowicz, M., Koletzko, B., Van Spronsen, F.J., Niezen-Koning, K.E., Matthijs, G., Gardeitchik, T., Kouwenberg, D., Lim, B.C., Zeevaert, R., Wevers, R.A., Lefeber, D.J., Morava, E., Clinical and diagnostic approach in unsolved CDG patients with a type 2 transferrin pattern. Biochim. Biophys. Acta 1812 (2011), 691–698.
35. Bahena-Bahena, D., López-Valdez, J., Raymond, K., Salinas-Marín, R., Ortega-García, A., Ng, B.G., Freeze, H.H., Ruíz-García, M., Martínez-Duncker, I., ATP6V0A2 mutations present in two Mexican Mestizo children with an autosomal recessive cutis laxa syndrome type IIA. Mol. Genet. Metab. Rep. 1 (2014), 203–212.
36. Stephensen, C.B., Vitamin A, infection, and immune function. Annu. Rev. Nutr. 21 (2001), 167–192.
37. Barua, A., Stacewicz-Sapuntzakis, M., Furr, H., Vitamin A - retinol. Herrmann, W., Obeid, R., (eds.) Vitamins in the Prevention of Human Diseases, 2011, Walter de Gruyter, New York, 7–39.
38. Chen, W., Chen, G., The roles of vitamin A in the regulation of carbohydrate, lipid, and protein metabolism. J. Clin. Med. 3 (2014), 453–479.
39. Holick, M.F., Sunlight and vitamin D for bone health and prevention of autoimmune diseases, cancers, and cardiovascular disease. Am. J. Clin. Nutr. 80 (2004), 1678S–1688S.
40. Clarke, M.W., Burnett, J.R., Croft, K.D., Vitamin E in human health and disease. Crit. Rev. Clin. Lab. Sci. 45 (2008), 417–450.
41. Plum, L.A., DeLuca, H.F., Vitamin D, disease and therapeutic opportunities. Nat. Rev. Drug Discov. 9 (2010), 941–955.
42. Beard, J.A., Bearden, A., Striker, R., Vitamin D and the anti-viral state. J. Clin. Virol. 50 (2011), 194–200.
43. Albahrani, A.A., Greaves, R.F., Fat-soluble vitamins: clinical indications and current challenges for chromatographic measurement. Clin. Biochem. Rev. 37 (2016), 27–47.
44. Yip, B., Chen, S.H., Mulder, H., Höppener, J.W., Schachter, H., Organization of the human beta-1,2-N-acetylglucosaminyltransferase I gene (MGAT1), which controls complex and hybrid N-glycan synthesis. Biochem. J. 321 (1997), 465–474.
45. Suraweera, A., Münch, C., Hanssum, A., Bertolotti, A., Failure of amino acid homeostasis causes cell death following proteasome inhibition. Mol. Cell 48 (2012), 242–253.
46. Matos, L., Gouveia, A.M., Almeida, H., ER stress response in human cellular models of senescence. J. Gerontol. A. Biol. Sc. Med. Sci. 70 (2015), 924–935.