Home LiteratureArticle Details
PMID: 18287059 Published · ppublish English Comparative Study Journal Article Research Support, Non-U.S. Gov't

Elevated globotriaosylsphingosine is a hallmark of Fabry disease.

Aerts JM, Groener JE, Kuiper S, Donker-Koopman WE, Strijland A, Ottenhoff R, van Roomen C, Mirzaian M, Wijburg FA, Linthorst GE, Vedder AC, Rombach SM, Cox-Brinkman J, Somerharju P, Boot RG, Hollak CE, Brady RO, Poorthuis BJ

Abstract

Fabry disease is an X-linked lysosomal storage disease caused by deficiency of alpha-galactosidase A that affects males and shows disease expression in heterozygotes. The characteristic progressive renal insufficiency, cardiac involvement, and neuropathology usually are ascribed to globotriaosylceramide accumulation in the endothelium. However, no direct correlation exists between lipid storage and clinical manifestations, and treatment of patients with recombinant enzymes does not reverse several key signs despite clearance of lipid from the endothelium. We therefore investigated the possibility that globotriaosylceramide metabolites are a missing link in the pathogenesis. We report that deacylated globotriaosylceramide, globotriaosylsphingosine, and a minor additional metabolite are dramatically increased in plasma of classically affected male Fabry patients and plasma and tissues of Fabry mice. Plasma globotriaosylceramide levels are reduced by therapy. We show that globotriaosylsphingosine is an inhibitor of alpha-galactosidase A activity. Furthermore, exposure of smooth muscle cells, but not fibroblasts, to globotriaosylsphingosine at concentrations observed in plasma of patients promotes proliferation. The increased intima-media thickness in Fabry patients therefore may be related to the presence of this metabolite. Our findings suggest that measurement of circulating globotriaosylsphingosine will be useful to monitor Fabry disease and may contribute to a better understanding of the disorder.

MeSH Terms
Adolescent Adult Animals Cell Proliferation/drug effects Child Fabry Disease/blood Glycolipids/blood,pharmacology Humans Male Mice Myocytes, Smooth Muscle/cytology Netherlands Pedigree Sphingolipids/blood,pharmacology alpha-Galactosidase/antagonists & inhibitors
Chemicals
Glycolipids Sphingolipids globotriaosyl lysosphingolipid alpha-Galactosidase
Authors & Affiliations
18 authors, click to expand affiliations / ORCID
Aerts Johannes M
Amsterdam Lysosome Center, Departments of Medical Biochemistry, Internal Medicine, and Paediatrics, Academic Medical Center, Meibergdreef 9, 1105 AZ, Amsterdam, The Netherlands. [email protected]
Groener Johanna E
Kuiper Sijmen
Donker-Koopman Wilma E
Strijland Anneke
Ottenhoff Roelof
van Roomen Cindy
Mirzaian Mina
Wijburg Frits A
Linthorst Gabor E
Vedder Anouk C
Rombach Saskia M
Cox-Brinkman Josanne
Somerharju Pentti
Boot Rolf G
Hollak Carla E
Brady Roscoe O
Poorthuis Ben J
References (41)
41 references, click to expand
  1. Fabry's disease: alpha-galactosidase deficiency.
    Science. 1970 Feb 27;167(3922):1268-9 PMID: 5411915
  2. Treatment of Fabry disease: outcome of a comparative trial with agalsidase alfa or beta at a dose of 0.2 mg/kg.
    PLoS One. 2007 Jul 11;2(7):e598 PMID: 17622343
  3. Fabry disease: twenty-three mutations including sense and antisense CpG alterations and identification of a deletional hot-spot in the alpha-galactosidase A gene.
    Hum Mol Genet. 1994 Oct;3(10):1795-9 PMID: 7531540
  4. Replacement therapy for inherited enzyme deficiency. Use of purified ceramidetrihexosidase in Fabry's disease.
    N Engl J Med. 1973 Jul 5;289(1):9-14 PMID: 4196713
  5. Accumulation of lysosphingolipids in tissues from patients with GM1 and GM2 gangliosidoses.
    J Neurochem. 1992 Oct;59(4):1452-8 PMID: 1402895
  6. Separation of plasma lipoproteins by density-gradient ultracentrifugation.
    Anal Biochem. 1975 May 12;65(1-2):42-9 PMID: 165752
  7. Increased carotid intima-media thickness in the absence of atherosclerotic plaques in an adult population with Fabry disease.
    Acta Paediatr Suppl. 2006 Apr;95(451):63-8 PMID: 16720468
  8. Enzyme replacement therapy in Fabry disease: a randomized controlled trial.
    JAMA. 2001 Jun 6;285(21):2743-9 PMID: 11386930
  9. Structural and functional changes in peripheral vasculature of Fabry patients.
    J Inherit Metab Dis. 2006 Oct;29(5):660-6 PMID: 16906474
  10. Recurrence of Fabry's disease in a renal allograft eleven years after successful renal transplantation.
    Transplantation. 1991 Apr;51(4):759-62 PMID: 1849671
  11. Is globotriaosylceramide a useful biomarker in Fabry disease?
    Acta Paediatr Suppl. 2005 Mar;94(447):51-4; discussion 37-8 PMID: 15895713
  12. Chemical pathology of Krabbe disease: the occurrence of psychosine and other neutral sphingoglycolipids.
    Adv Exp Med Biol. 1976;68:115-26 PMID: 937104
  13. Safety and efficacy of recombinant human alpha-galactosidase A replacement therapy in Fabry's disease.
    N Engl J Med. 2001 Jul 5;345(1):9-16 PMID: 11439963
  14. A rapid method of total lipid extraction and purification.
    Can J Biochem Physiol. 1959 Aug;37(8):911-7 PMID: 13671378
  15. Toxicity of glucosylsphingosine (glucopsychosine) to cultured neuronal cells: a model system for assessing neuronal damage in Gaucher disease type 2 and 3.
    Neurobiol Dis. 2003 Dec;14(3):595-601 PMID: 14678774
  16. Accumulation of glucosylceramide and glucosylsphingosine (psychosine) in cerebrum and cerebellum in infantile and juvenile Gaucher disease.
    J Neurochem. 1982 Sep;39(3):709-18 PMID: 7097276
  17. Recombinant enzyme therapy for Fabry disease: absence of editing of human alpha-galactosidase A mRNA.
    Am J Hum Genet. 2003 Jan;72(1):23-31 PMID: 12471562
  18. Vascular effects of sphingolipids.
    Acta Paediatr. 2007 Apr;96(455):44-8 PMID: 17391441
  19. Natural history of Fabry disease in females in the Fabry Outcome Survey.
    J Med Genet. 2006 Apr;43(4):347-52 PMID: 16227523
  20. Sphingosine 1-phosphate stimulates smooth muscle cell differentiation and proliferation by activating separate serum response factor co-factors.
    J Biol Chem. 2004 Oct 8;279(41):42422-30 PMID: 15292266
  21. Twenty five years of the "psychosine hypothesis": a personal perspective of its history and present status.
    Neurochem Res. 1998 Mar;23(3):251-9 PMID: 9482237
  22. The enzymatic synthesis of psychosine.
    J Biol Chem. 1960 Jan;235:45-51 PMID: 13810623
  23. alpha-Galactosidase A deficient mice: a model of Fabry disease.
    Proc Natl Acad Sci U S A. 1997 Mar 18;94(6):2540-4 PMID: 9122231
  24. Enzymatic defect in Fabry's disease. Ceramidetrihexosidase deficiency.
    N Engl J Med. 1967 May 25;276(21):1163-7 PMID: 6023233
  25. The Dutch Fabry cohort: diversity of clinical manifestations and Gb3 levels.
    J Inherit Metab Dis. 2007 Feb;30(1):68-78 PMID: 17206462
  26. Natural history of Fabry disease in affected males and obligate carrier females.
    J Inherit Metab Dis. 2001;24 Suppl 2:13-4; discussion 11-2 PMID: 11758673
  27. Krabbe disease: a galactosylsphingosine (psychosine) lipidosis.
    J Lipid Res. 1980 Jan;21(1):53-64 PMID: 7354254
  28. Manifestations of Fabry disease in placental tissue.
    J Inherit Metab Dis. 2006 Feb;29(1):106-11 PMID: 16601876
  29. The role of ceramide trihexoside (globotriaosylceramide) in the diagnosis and follow-up of the efficacy of treatment of Fabry disease: a review of the literature.
    Cardiovasc Hematol Agents Med Chem. 2006 Oct;4(4):289-97 PMID: 17073606
  30. B.C.P. Jansen Institute, University of Amsterdam, Amsterdam, The Netherlands.
    Acta Med Scand. 1976;200(4):249-56 PMID: 824932
  31. Enzyme therapy for Fabry disease: neutralizing antibodies toward agalsidase alpha and beta.
    Kidney Int. 2004 Oct;66(4):1589-95 PMID: 15458455
  32. Glucosylsphingosine accumulation in tissues from patients with Gaucher disease: correlation with phenotype and genotype.
    Mol Genet Metab. 2002 Aug;76(4):262-70 PMID: 12208131
  33. Influence of antibody formation on reduction of globotriaosylceramide (GL-3) in urine from Fabry patients during agalsidase beta therapy.
    Mol Genet Metab. 2007 Nov;92(3):271-3 PMID: 17689998
  34. Anomeric structure of ceramide digalactoside isolated from the kidney of a patient with Fabry's disease.
    Biochim Biophys Acta. 1972 Jan 27;260(1):88-92 PMID: 5012456
  35. HPLC for simultaneous quantification of total ceramide, glucosylceramide, and ceramide trihexoside concentrations in plasma.
    Clin Chem. 2007 Apr;53(4):742-7 PMID: 17332150
  36. Anderson-Fabry disease: clinical manifestations of disease in female heterozygotes.
    J Inherit Metab Dis. 2001 Dec;24(7):715-24 PMID: 11804208
  37. Cellular and tissue localization of globotriaosylceramide in Fabry disease.
    Virchows Arch. 2007 Oct;451(4):823-34 PMID: 17674039
  38. Monitoring enzyme replacement therapy in Fabry disease--role of urine globotriaosylceramide.
    J Inherit Metab Dis. 2005;28(1):21-33 PMID: 15702403
  39. Cardiac and vascular hypertrophy in Fabry disease: evidence for a new mechanism independent of blood pressure and glycosphingolipid deposition.
    Arterioscler Thromb Vasc Biol. 2006 Apr;26(4):839-44 PMID: 16469946
  40. Progressive accumulation of toxic metabolite in a genetic leukodystrophy.
    Science. 1984 May 18;224(4650):753-5 PMID: 6719111
  41. The relationship of vascular glycolipid storage to clinical manifestations of Fabry disease: a cross-sectional study of a large cohort of clinically affected heterozygous women.
    Medicine (Baltimore). 2005 Sep;84(5):261-268 PMID: 16148726
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2008-02-26
Epub
2008-00-19
Pages
2812-7
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC2268542
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]