Gaucher disease: a model disorder for biomarker discovery

References

• Gieselmann V. Lysosomal storage diseases. Biochim. Biophys. Acta1270, 103–136 (1995).
   PubMed Web of Science ®Google Scholar
• Beutler E, Grabowski GA. Gaucher Disease. In: The Metabolic and Molecular Bases of Inherited Disease. Scriver CR, Sly WS, Childs B, Beaudet AL, Valle D, Kinzler KW, Vogelstein B (Eds). McGraw>–Hill Inc., NY, USA, 3635–3668 (2001).
   Google Scholar
• Patrick AD. A deficiency of glucocerebrosidase in Gaucher’s disease. Biochem. J.97, 17C–18C (1965).
   Google Scholar
• Brady RO, Kanfer JN, Bradley RM, Shapiro D. Demonstration of a deficiency of glucocerebroside-cleaving enzyme in Gaucher’s disease. J. Clin. Invest.45, 1112–1115 (1966).
   PubMed Web of Science ®Google Scholar
• Aerts JM, Donker-Koopman WE, van Vliet M et al. The occurrence of two immunologically distinguishable forms of glucocerebrosidase in human spleen. Eur. J. Biochem.150, 565–574 (1985).
   PubMedGoogle Scholar
• Aerts JM, Donker-Koopman WE, Koot M, Barranger JA, Tager JM, Schram AW. Deficient activity of glucocerebrosidase in urine from patients with type 1 Gaucher disease. Clin. Chim. Acta158, 155–164 (1986).
   PubMed Web of Science ®Google Scholar
• Sidransky E. Gaucher disease: complexity in a “simple” disorder. Mol. Genet. Metab.83, 6–15 (2004).
   PubMed Web of Science ®Google Scholar
• Jonsson LM, Murray GJ, Sorrell SH et al. Biosynthesis and maturation of glucocerebrosidase in Gaucher fibroblasts. Eur. J. Biochem.164, 171–179 (1987).
   PubMedGoogle Scholar
• Van Weely S, van Leeuwen M, Jansen D et al. Clinical genotype of Gaucher disease in relation to properties of mutant glucocerebrosidase in cultured fibroblasts. Biochim. Biophys. Acta1096, 301–311 (1991).
   PubMed Web of Science ®Google Scholar
• Aerts JM, Schram AW, Strijland A et al. Glucocerebrosidase, a lysosomal enzyme that does not undergo oligosaccharide phosphorylation. Biochim. Biophys. Acta964, 303–308 (1988).
   PubMed Web of Science ®Google Scholar
• Rijnboutt S, Aerts JM, Geuze HJ, Tager JM, Strous GJ. Mannose-6-phosphate independent membrane association of cathepsin D, glucocerebrosidase and sphingolipid activator protein in HepG2 cells. J. Biol. Chem.266, 4862–4868 (1991).
   PubMed Web of Science ®Google Scholar
• Reczek D, Schwake M, Schröder J et al. LIMP-2 is a receptor for lysosomal mannose-6-phosphate-independent targeting of β-glucocerebrosidase. Cell131, 770–783 (2007).
   PubMed Web of Science ®Google Scholar
• Balreira A, Gaspar P, Caiola D et al. A nonsense mutation in the LIMP-2 gene associated with progressive myoclonic epilepsy and nephrotic syndrome. Hum. Mol. Genet.17, 2238–2243 (2008).
   PubMed Web of Science ®Google Scholar
• Tylki-Szymańska A, Czartoryska B, Vanier MT et al. Non-neuronopathic Gaucher disease due to saposin C deficiency. Clin. Genet.72, 538–542 (2007).
   PubMed Web of Science ®Google Scholar
• Boot RG, Hollak CEM, Verhoek M et al. Glucocerebrosidase genotype of Gaucher patients in The Netherlands: limitations in prognostic value. Hum. Mut.10, 348–358 (1997).
   PubMed Web of Science ®Google Scholar
• Aerts JM, van Weely S, Boot R, Hollak CE, Tager JM. The pathogenesis of lysosomal storage disorders as illustrated by Gaucher disease. J. Inher. Met. Dis.16, 288–291 (1993).
   PubMed Web of Science ®Google Scholar
• Cox TM, Schofield JP. Gaucher’s disease: clinical features and natural history. Baillieres Clin. Hematol.10, 657–689 (1997).
   PubMed Web of Science ®Google Scholar
• Lachmann RH, Grant IR, Halsall D, Cox TM. Twin pairs showing discordance of phenotype in adult Gaucher’s disease. QJM97, 199–204 (2004).
   PubMed Web of Science ®Google Scholar
• van Weely S, Brandsma M, Strijland A, Tager JM, Aerts JM. Demonstration of the existence of a second, non-lysosomal glucocerebrosidase that is not deficient in Gaucher disease. Biochim. Biophys. Acta1181, 55–62 (1993).
   PubMed Web of Science ®Google Scholar
• Boot RG, Verhoek M, Donker-Koopman W et al. Identification of the non-lysosomal glucosylceramidase as β-glucosidase 2. J. Biol. Chem.282, 1305–1312 (2007).
   PubMed Web of Science ®Google Scholar
• Yildiz Y, Matern H, Thompson B et al. Mutation of β-glucosidase 2 causes glycolipid storage disease and impaired male fertility. J. Clin. Invest.116, 2985–2994 (2006).
   PubMed Web of Science ®Google Scholar
• Boven LA, van Meurs M, Boot RG, Mehta A, Aerts JM, Laman JD. Gaucher cells demonstrate a distinct macrophage phenotype and resemble alternatively activated macrophages. Am. J. Clin. Pathol.122, 359–369 (2004).
   PubMed Web of Science ®Google Scholar
• van Breemen MJ, de Fost M, Voerman JS et al. Increased plasma macrophage inflammatory protein (MIP)-1α and MIP-1β levels in type 1 Gaucher disease. Biochim. Biophys. Acta1772, 788–796 (2007).
   PubMed Web of Science ®Google Scholar
• Michelakakis H, Spanou C, Kondyli A et al. Plasma tumor necrosis factor-α (TNF-α) levels in Gaucher disease. Biochim. Biophys. Acta1317, 219–222 (1996)
   PubMed Web of Science ®Google Scholar
• Hollak CE, Evers L, Aerts JM, van Oers MH. Elevated levels of M-CSF, sCD14 and IL8 in type 1 Gaucher disease. Blood Cells Mol. Dis.23, 201–212 (1997).
   PubMed Web of Science ®Google Scholar
• Hollak CE, Levi M, Berends F, Aerts JM, van Oers MH. Coagulation abnormalities in type 1 Gaucher disease are due to low-grade activation and can be partly restored. Br. J. Hematol.96, 470–476 (1997).
   PubMed Web of Science ®Google Scholar
• Aerts JM, Hollak CE. Plasma and metabolic abnormalities in Gaucher’s disease. Baillieres Clin. Haematol.10, 691–709 (1997).
   PubMed Web of Science ®Google Scholar
• Boot RG, Verhoek M, de Fost M et al. Marked elevation of the chemokine CCL18/PARC in Gaucher disease: a novel surrogate marker for assessing therapeutic intervention. Blood103, 33–39 (2004).
   PubMed Web of Science ®Google Scholar
• Cox TM. Gaucher disease: understanding the molecular pathogenesis of sphingolipidoses. J. Inherit. Met. Dis.24(Suppl. 2), 106–121 (2001).
   PubMed Web of Science ®Google Scholar
• Moran MT, Schofield JP, Hayman AR, Shi GP, Young E, Cox TM. Pathologic gene expression in Gaucher disease: up-regulation of cysteine proteinases including osteoclastic cathepsin K. Blood96, 1969–1978 (2000).
   PubMed Web of Science ®Google Scholar
• Moller HJ, de Fost M, Aerts H, Hollak CE, Moestrup SK. Soluble haemoglobin scavenger receptor CD163: a macrophage specific marker in Gaucher disease. Eur. J. Haematol.72, 135–139 (2004).
   PubMed Web of Science ®Google Scholar
• Barton NW, Furbish FS, Murray GJ, Garfield M, Brady RO. Therapeutic response to intravenous infusions of glucocerebrosidase in a patient with Gaucher disease. Proc. Natl Acad. Sci. USA87, 1913–1916 (1990).
   PubMed Web of Science ®Google Scholar
• Cox T, Lachmann R, Hollak CE et al. Novel oral treatment of Gaucher’s disease with N-butyldeoxynojirimycin (OGT918) to decrease substrate biosynthesis. Lancet355, 1481–1485 (2000).
   PubMed Web of Science ®Google Scholar
• Aerts JM, Hollak CE, Boot RG, Groener JE, Maas M. Substrate reduction therapy of glycosphingolipid storage disorders. J. Inherit. Metab. Dis.29, 449–456 (2006).
   PubMed Web of Science ®Google Scholar
• Cox TM, Aerts JM, Andria G et al. Advisory Council to the European Working Group on Gaucher Disease. The role of the iminosugar N-butyldeoxynojirimycin (miglustat) in the management of type I (non-neuronopathic) Gaucher disease: a position statement. J. Inherit. Metab. Dis.26, 513–526 (2003).
   PubMed Web of Science ®Google Scholar
• Butters TD. Gaucher disease. Curr. Opin. Chem. Biol.11, 412–418 (2007).
   PubMed Web of Science ®Google Scholar
• Yu Z, Sawkar AR, Kelly JW. Pharmacologic chaperoning as a strategy to treat Gaucher disease. FEBS J.274, 4944–4950 (2007).
   PubMed Web of Science ®Google Scholar
• Bussink AP, van Eijk M, Renkema GH, Aerts JM, Boot RG. The biology of the Gaucher cell: the cradle of human chitinases. Int. Rev. Cytol.252, 71–128 (2006).
   PubMedGoogle Scholar
• Hollak CE, van Weely S, van Oers MH, Aerts JM. Marked elevation of plasma chitotriosidase activity. A novel hallmark of Gaucher disease. J. Clin. Invest.93, 1288–1292 (1994).
   PubMed Web of Science ®Google Scholar
• Renkema GH, Boot RG, Muijsers AO, Donker-Koopman WE, Aerts JM. Purification and characterization of human chitotriosidase, a novel member of the chitinase family of proteins. J. Biol. Chem.270, 2198–2202 (1995).
   PubMed Web of Science ®Google Scholar
• Boot RG, Renkema GH, Strijland A, van Zonneveld AJ, Aerts JM. Cloning of a cDNA encoding chitotriosidase, a human chitinase produced by macrophages. J. Biol. Chem.270, 26252–26256. (1995).
   PubMed Web of Science ®Google Scholar
• Renkema GH, Boot RG, Strijland A et al. Synthesis, sorting and processing into distinct isoforms of human macrophage chitotriosidase. Eur. J. Biochem.244, 279–285 (1997).
   PubMedGoogle Scholar
• Ghauharali-van der Vlugt K, Bussink AP, Groener JE, Boot RG, Aerts JM. Detection of chitinase activity by 2-aminobenzoic acid labeling of chito-oligosaccharides. Anal. Biochem.384, 191–193 (2009).
   PubMed Web of Science ®Google Scholar
• Aguilera B, Ghauharali-van der Vlugt K, Helmond MT et al. Transglycosidase activity of chitotriosidase: improved enzymatic assay for the human macrophage chitinase. J. Biol. Chem.278, 40911–40916 (2003).
   PubMed Web of Science ®Google Scholar
• Boot RG, Renkema GH, Verhoek M et al. The human chitotriosidase gene. Nature of inherited enzyme deficiency. J. Biol. Chem.273, 25680–25685 (1998).
   PubMed Web of Science ®Google Scholar
• Schoonhoven A, Rudensky B, Elstein D et al. Monitoring of Gaucher patients with a novel chitotriosidase assay. Clin. Chim. Acta381, 136–139 (2007).
   PubMed Web of Science ®Google Scholar
• de Fost M, Hollak CE, Groener JE et al. Superior effects of high-dose enzyme replacement therapy in type 1 Gaucher disease on bone marrow involvement and chitotriosidase levels: a 2-center retrospective analysis. Blood108, 830–835 (2006).
   PubMed Web of Science ®Google Scholar
• Grace ME, Balwani M, Nazarenko I, Prakash-Cheng A, Desnick RJ. Type 1 Gaucher disease: null and hypomorphic novel chitotriosidase mutations-implications for diagnosis and therapeutic monitoring. Hum Mutat.28, 866–873 (2007).
   PubMed Web of Science ®Google Scholar
• Lee P, Waalen J, Crain K, Smargon A, Beutler E. Human chitotriosidase polymorphisms G354R and A442V associated with reduced enzyme activity. Blood Cells Mol. Dis.39, 353–360 (2007).
   PubMed Web of Science ®Google Scholar
• Guo Y, He W, Boer AM et al. Elevated plasma chitotriosidase activity in various lysosomal storage disorders. J. Inherit. Metab. Dis.18, 717–722 (1995).
   PubMed Web of Science ®Google Scholar
• Ries M, Schaefer E, Lührs T et al. Critical assessment of chitotriosidase analysis in the rational laboratory diagnosis of children with Gaucher disease and Niemann–Pick disease type A/B and C. J. Inherit. Metab. Dis.29, 647–652 (2006).
   PubMed Web of Science ®Google Scholar
• Wajner A, Michelin K, Burin MG et al. Biochemical characterization of chitotriosidase enzyme: comparison between normal individuals and patients with Gaucher and with Niemann–Pick diseases. Clin. Biochem.37, 893–897 (2004).
   PubMed Web of Science ®Google Scholar
• Wajner A, Michelin K, Burin MG et al. Comparison between the biochemical properties of plasma chitotriosidase from normal individuals and from patients with Gaucher disease, GM1-gangliosidosis, Krabbe disease and heterozygotes for Gaucher disease. Clin. Biochem.40, 365–369 (2007).
   PubMed Web of Science ®Google Scholar
• vom Dahl S, Harzer K, Rolfs A et al. Hepatosplenomegalic lipidosis: what unless Gaucher? Adult cholesteryl ester storage disease (CESD) with anemia, mesenteric lipodystrophy, increased plasma chitotriosidase activity and a homozygous lysosomal acid lipase -1 exon 8 splice junction mutation. J. Hepatol.31, 741–746 (1999).
   PubMed Web of Science ®Google Scholar
• Vedder AC, Cox-Brinkman J, Hollak CE et al. Plasma chitotriosidase in male Fabry patients: a marker for monitoring lipid-laden macrophages and their correction by enzyme replacement therapy. Mol. Genet. Metab.89, 239–244 (2006).
   PubMed Web of Science ®Google Scholar
• Brinkman J, Wijburg FA, Hollak CE et al. Plasma chitotriosidase and CCL18: early biochemical surrogate markers in type B Niemann–Pick disease. J. Inherit. Metab. Dis.28, 13–20 (2005).
   PubMed Web of Science ®Google Scholar
• Michelakakis H, Dimitriou E, Labadaridis I. The expanding spectrum of disorders with elevated plasma chitotriosidase activity: an update. J. Inherit. Metab. Dis.27, 705–706 (2004).
   PubMed Web of Science ®Google Scholar
• Grosso S, Margollicci MA, Bargagli E et al. Serum levels of chitotriosidase as a marker of disease activity and clinical stage in sarcoidosis. Scand. J. Clin. Lab. Invest.64, 57–62 (2004)
   PubMed Web of Science ®Google Scholar
• Iyer A, van Eijk M, Silva E et al. Increased chitotriosidase activity in serum of leprosy patients: association with bacillary leprosy. Clin. Immunol.131(3), 501–509 (2009).
   PubMed Web of Science ®Google Scholar
• Brunner JK, Scholl-Bürgi S, Hössinger D, Wondrak P, Prelog M, Zimmerhackl LB. Chitotriosidase activity in juvenile idiopathic arthritis. Rheumatol. Int.28, 949–950 (2008).
   PubMed Web of Science ®Google Scholar
• Sotgiu S, Barone R, Arru G et al. Intrathecal chitotriosidase and the outcome of multiple sclerosis. Mult. Scler.12, 551–557 (2006).
   PubMed Web of Science ®Google Scholar
• Barone R, Di Gregorio F, Romeo MA, Schilirò G, Pavone L. Plasma chitotriosidase activity in patients with β-thalassemia. Blood Cells Mol. Dis.25, 1–8 (1999).
   PubMed Web of Science ®Google Scholar
• Barone R, Simporé J, Malaguarnera L, Pignatelli S, Musumeci S. Plasma chitotriosidase activity in acute Plasmodium falciparum malaria. Clin. Chim. Acta331, 79–85 (2003).
   PubMed Web of Science ®Google Scholar
• Artieda M, Cenarro A, Gañán A et al. Serum chitotriosidase activity is increased in subjects with atherosclerosis disease. Arterioscler. Thromb. Vasc. Biol.23, 1645–1652 (2003).
   PubMed Web of Science ®Google Scholar
• Boot RG, van Achterberg TA, van Aken BE et al. Strong induction of members of the chitinase family of proteins in atherosclerosis: chitotriosidase and human cartilage gp-39 expressed in lesion macrophages. Arterioscler. Thromb. Vasc. Biol.19, 687–694 (1999).
   PubMed Web of Science ®Google Scholar
• Seibold MA, Donnelly S, Solon M et al. Chitotriosidase is the primary active chitinase in the human lung and is modulated by genotype and smoking habit. J. Allergy Clin. Immunol.122, 944–950 (2008).
   PubMed Web of Science ®Google Scholar
• van Breemen MJ, Bleijlevens B, de Koster CG, Aerts JM. Limitations in quantitation of the biomarker CCL18 in Gaucher disease blood samples by surface-enhanced laser desorption/ionization time-of-flight mass spectrometry. Biochim. Biophys. Acta1764, 1626–1632 (2006).
   PubMed Web of Science ®Google Scholar
• Deegan PB, Moran MT, McFarlane I et al. Clinical evaluation of chemokine and enzymatic biomarkers of Gaucher disease. Blood Cells Mol. Dis.35, 259–267 (2005).
   PubMed Web of Science ®Google Scholar
• Boot RG, Verhoek M, Langeveld M et al. CCL18: a urinary marker of Gaucher cell burden in Gaucher patients. J. Inherit. Metab. Dis.29, 564–571 (2006).
   PubMed Web of Science ®Google Scholar
• Maas M, Hollak CE, Akkerman EM, Aerts JM, Stoker J, Den Heeten GJ. Quantification of skeletal involvement in adults with type I Gaucher’s disease: fat fraction measured by Dixon quantitative chemical shift imaging as a valid parameter. AJR Am. J. Roentgenol.179, 961–965 (2002).
   PubMed Web of Science ®Google Scholar
• Hollak CE, Maas M, Aerts JM. Clinically relevant therapeutic endpoints in type I Gaucher disease. J. Inherit. Metab. Dis.24(Suppl. 2), 97–105 (2001).
   PubMed Web of Science ®Google Scholar
• Zimran A, Elstein D, Beutler E. Low-dose therapy trumps high-dose therapy again in the treatment of Gaucher disease. Blood108, 802–803 (2006).
   PubMed Web of Science ®Google Scholar
• Zimran CE, de Fost M, Aerts JM, vom Dahl S. Low-dose versus high-dose therapy for Gaucher disease: goals and markers. Blood109, 387 (2007).
   PubMed Web of Science ®Google Scholar
• Zimran A, Ilan Y, Elstein D. Enzyme replacement therapy for mild patients with Gaucher disease. Am. J. Hematol.84, 202–204 (2009).
   PubMed Web of Science ®Google Scholar
• Mistry PK, Weinreb NJ, Brady RO, Grabowski GA. Gaucher disease: resetting the clinical and scientific agenda. Am. J. Hematol.84, 205–207 (2009).
   PubMed Web of Science ®Google Scholar
• Groener JE, Poorthuis BJ, Kuiper S, Helmond MT, Hollak CE, Aerts JM. HPLC for simultaneous quantification of total ceramide, glucosylceramide, and ceramide trihexoside concentrations in plasma. Clin. Chem.53, 742–747 (2007).
   PubMed Web of Science ®Google Scholar
• Ghauharali-van der Vlugt K, Langeveld M, Poppema A et al. Prominent increase in plasma ganglioside GM3 is associated with clinical manifestations of type I Gaucher disease. Clin. Chim. Acta389, 109–113 (2007).
   PubMed Web of Science ®Google Scholar
• Aerts JM, Ottenhoff R, Powlson AS et al. Pharmacological inhibition of glucosylceramide synthase enhances insulin sensitivity. Diabetes56, 1341–1349 (2007).
   PubMed Web of Science ®Google Scholar
• Langeveld M, de Fost M, Aerts JM, Sauerwein HP, Hollak CE. Overweight, insulin resistance and Type II diabetes in type I Gaucher disease patients in relation to enzyme replacement therapy. Blood Cells Mol. Dis.40, 428–432 (2008).
   PubMed Web of Science ®Google Scholar
• Anderson L. Candidate-based proteomics in the search for biomarkers of cardiovascular disease. J. Physiol.563, 23–60 (2005).
   PubMed Web of Science ®Google Scholar
• van Breemen MJ, Aerts JM, Sprenger RR, Speijer D. Potential artefacts in proteome analysis of plasma of Gaucher patients due to protease abnormalities. Clin. Chim. Acta396, 26–32 (2008).
   PubMed Web of Science ®Google Scholar
• Smit S, van Breemen MJ, Hoefsloot HC, Smilde AK, Aerts JM, de Koster CG. Assessing the statistical validity of proteomics based biomarkers. Anal. Chim. Acta592, 210–217 (2007).
   PubMed Web of Science ®Google Scholar
• Silva JC, Gorenstein MV, Li GZ, Vissers JP, Geromanos SJ. Absolute quantification of proteins by LCMSE; a virtue of parallel MS acquisition. Mol. Cell Proteomics5, 144–156 (2006).
   PubMed Web of Science ®Google Scholar
• Vissers JP, Langridge JI, Aerts JM. Analysis and quantification of diagnostic serum markers and protein signatures for Gaucher disease. Mol. Cell Proteomics6, 755–766 (2007).
   PubMed Web of Science ®Google Scholar
• Fusetti F, von Moeller H, Houston D et al. Structure of human chitotriosidase. Implications for specific inhibitor design and function of mammalian chitinase-like lectins. J. Biol. Chem.277, 25537–25544 (2002).
   PubMed Web of Science ®Google Scholar
• Rao FV, Houston DR, Boot RG, Aerts JM, Sakuda S, van Aalten DM. Crystal structures of allosamidin derivatives in complex with human macrophage chitinase. J. Biol. Chem.278, 20110–20116 (2003).
   PubMed Web of Science ®Google Scholar
• van Eijk M, van Roomen CP, Renkema GH et al. Characterization of human phagocyte-derived chitotriosidase, a component of innate immunity. Int. Immunol.17, 1505–1512 (2005).
   PubMed Web of Science ®Google Scholar