1,552
Views
6
CrossRef citations to date
0
Altmetric
Research Article

Glycosphingolipid Storage in Fabry Mice Extends Beyond Globotriaosylceramide and is Affected by ABCB1 Depletion

, , , , , , , , , , & show all
Article: FSO147 | Accepted 10 Aug 2016, Published online: 13 Oct 2016

References

  • Brady RO, Gal AE, Bradley RM, Martensson E, Warshaw AL, Laster L. Enzymatic defect in Fabry’s disease. Ceramidetrihexosidase deficiency. N. Engl. J. Med. 276(21), 1163–1167 (1967).
  • Lidove O, Joly D, Barbey F et al. Clinical results of enzyme replacement therapy in Fabry disease: a comprehensive review of literature. Int. J. Clin. Pract. 61(2), 293–302 (2007).
  • Motabar O, Sidransky E, Goldin E, Zheng W. Fabry disease – current treatment and new drug development. Curr. Chem. Genomics 4(1), 50–56 (2010).
  • Vedder AC, Linthorst GE, van Breemen MJ et al. The Dutch Fabry cohort: diversity of clinical manifestations and Gb3 levels. J. Inherit. Metab. Dis. 30(1), 68–78 (2007).
  • Aerts JM. Elevated globotriaosylsphingosine is a hallmark of Fabry disease. Proc. Natl Acad. Sci. USA 105(8), 2812–2817 (2008).
  • Grösch S, Schiffmann S, Geisslinger G. Chain length-specific properties of ceramides. Prog. Lipid Res. 51(1), 50–62 (2012).
  • Mullen TD, Hannun YA, Obeid LM. Ceramide synthases at the centre of sphingolipid metabolism and biology. Biochem. J. 441(3), 789–802 (2012).
  • Köberlin MS, Snijder B, Heinz LX et al. A conserved circular network of coregulated lipids modulates innate immune responses. Cell 162(1), 170–183 (2015).
  • Levy M, Futerman AH. Mammalian ceramide synthases. IUBMB Life 62(5), 347–356 (2010).
  • Ohshima T, Murray GJ, Swaim WD et al. α-Galactosidase A deficient mice: a model of fabry disease. Proc. Natl Acad. Sci. USA 94(6), 2540–2544 (1997).
  • Ohshima T, Schiffmann R, Murray GJ et al. Aging accentuates and bone marrow transplantation ameliorates metabolic defects in Fabry disease mice. Proc. Natl Acad. Sci. USA 96(11), 6423–6427 (1999).
  • Dekker N, Van Dussen L, Hollak CEM et al. Elevated plasma glucosylsphingosine in Gaucher disease: relation to phenotype, storage cell markers, and therapeutic response. Blood 118(16), e118–e127 (2011).
  • Xu S, Lun Y, Brignol N et al. Coformulation of a novel human α-galactosidase A with the pharmacological chaperone AT1001 leads to improved substrate reduction in Fabry mice. Mol. Ther. 23(7), 1169–1181 (2015).
  • Kizhner T, Azulay Y, Hainrichson M et al. Characterization of a chemically modified plant cell culture expressed human α-galactosidase-A enzyme for treatment of Fabry disease. Mol. Genet. Metab. 114(2), 259–267 (2015).
  • Porubsky S, Jennemann R, Lehmann L, Gröne H-J. Depletion of globosides and isoglobosides fully reverts the morphologic phenotype of Fabry disease. Cell Tissue Res. 358(1), 217–227 (2014).
  • Yokoi T, Kobayashi H, Shimada Y et al. Minimum requirement of donor cells to reduce the glycolipid storage following bone marrow transplantation in a murine model of Fabry disease. J. Gene Med. 13(5), 262–268 (2011).
  • Shen J-S, Meng X-L, Wight-Carter M et al. Blocking hyperactive androgen receptor signaling ameliorates cardiac and renal hypertrophy in Fabry mice. Hum. Mol. Genet. 24(11), 3181–3191 (2015).
  • Moore DF, Ries M, Forget EL, Schiffmann R. Enzyme replacement therapy in orphan and ultra-orphan diseases: the limitations of standard economic metrics as exemplified by Fabry-Anderson disease. Pharmacoeconomics 25(3), 201–208 (2007).
  • Vedder AC, Linthorst GE, Houge G et al. Treatment of Fabry disease: outcome of a comparative trial with agalsidase alfa or beta at a dose of 0.2 mg/kg. PLoS ONE 2(7), e598 (2007).
  • Lidove O, West ML, Pintos-Morell G et al. Effects of enzyme replacement therapy in Fabry disease-a comprehensive review of the medical literature. Genet. Med. 12(11), 668–679 (2010).
  • Rombach SM, Smid BE, Linthorst GE, Dijkgraaf MGW, Hollak CEM. Natural course of Fabry disease and the effectiveness of enzyme replacement therapy: a systematic review and meta-analysis: effectiveness of ERT in different disease stages. J. Inherit. Metab. Dis. 37(3), 341–352 (2014).
  • Kato A, Yamashita Y, Nakagawa S et al. 2,5-Dideoxy-2,5-imino-D-altritol as a new class of pharmacological chaperone for Fabry disease. Bioorg. Med. Chem. 18(11), 3790–3794 (2010).
  • Khanna R, Soska R, Lun Y et al. The pharmacological chaperone 1-deoxygalactonojirimycin reduces tissue globotriaosylceramide levels in a mouse model of Fabry disease. Mol. Ther. 18(1), 23–33 (2010).
  • Yoshimitsu M, Higuchi K, Ramsubir S et al. Efficient correction of Fabry mice and patient cells mediated by lentiviral transduction of hematopoietic stem/progenitor cells. Gene Ther. 14(3), 256–265 (2007).
  • Marshall J, Ashe KM, Bangari D et al. Substrate reduction augments the efficacy of enzyme therapy in a mouse model of Fabry disease. PLoS ONE 5(11), e15033 (2010).
  • Mattocks M. Treatment of neutral glycosphingolipid lysosomal storage diseases via inhibition of the ABC drug transporter, MDR1. Cyclosporin A can lower serum and liver globotriaosyl ceramide levels in the Fabry mouse model. FEBS J. 273(9), 2064 (2006).
  • Gottesman MM, Pastan I. Biochemistry of multidrug resistance mediated by the multidrug transporter. Annu. Rev. Biochem. 62, 385–427 (1993).
  • Ueda K. ABC proteins protect the human body and maintain optimal health. Biosci. Biotechnol. Biochem. 75(3), 401–409 (2011).
  • Thiebaut F, Tsuruo T, Hamada H, Gottesman MM, Pastan I, Willingham MC. Cellular localization of the multidrug-resistance gene product P-glycoprotein in normal human tissues. Proc. Natl Acad. Sci. USA 84(21), 7735–7738 (1987).
  • Cascorbi I. P-glycoprotein: tissue distribution, substrates, and functional consequences of genetic variations. Handb. Exp. Pharmacol. 201, 261–283 (2011).
  • Fromm MF. Importance of P-glycoprotein at blood-tissue barriers. Trends Pharmacol. Sci. 25(8), 423–429 (2004).
  • Molinari A, Cianfriglia M, Meschini S, Calcabrini A, Arancia G. P-glycoprotein expression in the Golgi apparatus of multidrug-resistant cells. Int. J. Cancer 59(6), 789–795 (1994).
  • Lala P, Ito S, Lingwood CA. Retroviral transfection of Madin-Darby canine kidney cells with human MDR1 results in a major increase in globotriaosylceramide and 105- to 106-fold increased cell sensitivity to verocytotoxin. Role of P-glycoprotein in glycolipid synthesis. J. Biol. Chem. 275(9), 6246–6251 (2000).
  • Buton X, Hervé P, Kubelt J et al. Transbilayer movement of monohexosylsphingolipids in endoplasmic reticulum and Golgi membranes. Biochemistry 41(43), 13106–13115 (2002).
  • De Rosa MF, Sillence D, Ackerley C, Lingwood C. Role of multiple drug resistance protein 1 in neutral but not acidic glycosphingolipid biosynthesis. J. Biol. Chem. 279(9), 7867–7876 (2004).
  • Eckford PDW, Sharom FJ. The reconstituted P-glycoprotein multidrug transporter is a flippase for glucosylceramide and other simple glycosphingolipids. Biochem. J. 389(2), 517–526 (2005).
  • Mizutani T, Hattori A. New horizon of MDR1 (P-glycoprotein) study. Drug Metab. Rev. 37(3), 489–510 (2005).
  • Coste H, Martel MB, Got R. Topology of glucosylceramide synthesis in Golgi membranes from porcine submaxillary glands. Biochim. Biophys. Acta 858(1), 6–12 (1986).
  • Jeckel D, Karrenbauer A, Burger KNJ, Van Meer G, Wieland F. Glucosylceramide is synthesized at the cytosolic surface of various Golgi subfractions. J. Cell Biol. 117(2), 259–267 (1992).
  • Jeckel D. Lactosylceramide is synthesized in the lumen of the Golgi apparatus. FEBS Lett. 342(1), 91–96 (1994).
  • Yoshimitsu M, Sato T, Tao K et al. Bioluminescent imaging of a marking transgene and correction of Fabry mice by neonatal injection of recombinant lentiviral vectors. Proc. Natl Acad. Sci. USA 101(48), 16909–16914 (2004).
  • Mayes JS, Scheerer JB, Sifers RN, Donaldson ML. Differential assay for lysosomal alpha-galactosidases in human tissues and its application to Fabry’s disease. Clin. Chim. Acta. 112(2), 247–251 (1981).
  • Andrade J, Waters PJ, Singh RS et al. Screening for Fabry disease in patients with chronic kidney disease: limitations of plasma alpha-galactosidase assay as a screening test. Clin. J. Am. Soc. Nephrol. 3(1), 139–145 (2008).
  • Manwaring V, Boutin M, Auray-Blais C. A metabolomic study to identify new globotriaosylceramide-related biomarkers in the plasma of fabry disease patients. Anal. Chem. 85(19), 9039–9048 (2013).
  • Auray-Blais C, Boutin M. Novel Gb3 isoforms detected in urine of Fabry disease patients: a metabolomic study. Curr. Med. Chem. 19(19), 3241–3252 (2012).
  • Petric M, Karmali MA, Richardson S, Cheung R. Purification and biological properties of Escherichia coli verocytotoxin. FEMS Microbiol. Lett. 41(1), 63–68 (1987).
  • Ottico E, Prinetti A, Prioni S et al. Dynamics of membrane lipid domains in neuronal cells differentiated in culture. J. Lipid Res. 44(11), 2142–2151 (2003).
  • Boyd B, Richardson S, Gariepy J. Serological responses to the B subunit of Shiga-like toxin 1 and its peptide fragments indicate that the B subunit is a vaccine candidate to counter the action of the toxin. Infect. Immun. 59(3), 750–757 (1991).
  • Fisher RA. Frequency distribution of the values of the correlation coefficient in samples from an indefinitely large population. Biometrika 10(4), 507–521 (1915).
  • D’Angelo G. Glycosphingolipid synthesis requires FAPP2 transfer of glucosylceramide. Nature 449(7158), 62–67 (2007).
  • Halter D. Pre- and post-Golgi translocation of glucosylceramide in glycosphingolipid synthesis. J. Cell Biol. 179(1), 101–115 (2007).
  • Lingwood D, Binnington B, Rog T et al. Cholesterol modulates glycolipid conformation and receptor activity. Nat. Chem. Biol. 7(5), 260–262 (2011).
  • Taguchi A, Maruyama H, Nameta M et al. A symptomatic Fabry disease mouse model generated by inducing globotriaosylceramide synthesis. Biochem. J. 456(3), 373–83 (2013).
  • Kuchar L, Faltyskova H, Krasny L et al. Fabry disease: renal sphingolipid distribution in the α-Gal A knockout mouse model by mass spectrometric and immunohistochemical imaging. Anal. Bioanal. Chem. 407(8), 2283–2291 (2014).
  • Durant B, Forni S, Sweetman L et al. Sex differences of urinary and kidney globotriaosylceramide and lyso-globotriaosylceramide in Fabry mice. J. Lipid Res. 52(9), 1742–1746 (2011).
  • Aureli M, Grassi S, Prioni S, Sonnino S, Prinetti A. Lipid membrane domains in the brain. Biochim. Biophys. Acta 1851(8), 1006–1016 (2015).
  • Lingwood CA, Binnington B, Manis A, Branch DR. Globotriaosyl ceramide receptor function - where membrane structure and pathology intersect. FEBS Lett. 584(9), 1879–86 (2010).
  • Nutikka A, Lingwood C. Generation of receptor-active, globotriaosyl ceramide/cholesterol lipid “rafts” in vitro: A new assay to define factors affecting glycosphingolipid receptor activity. Glycoconj. J. 20(1), 33–38 (2004).
  • Jorissen RN, Walker F, Pouliot N, Garrett TPJ, Ward CW, Burgess AW. Epidermal growth factor receptor: mechanisms of activation and signalling. Exp. Cell Res. 284(1), 31–53 (2003).
  • Yoon S-J. Epidermal growth factor receptor tyrosine kinase is modulated by GM3 interaction with N-linked GlcNAc termini of the receptor. Proc. Natl Acad. Sci. USA 103(50), 18987–18991 (2006).
  • Kabayama K, Sato T, Saito K et al. Dissociation of the insulin receptor and caveolin-1 complex by ganglioside GM3 in the state of insulin resistance. Proc. Natl Acad. Sci. USA 104(34), 13678–13683 (2007).
  • Fuller M, Sharp PC, Rozaklis T et al. Urinary lipid profiling for the identification of fabry hemizygotes and heterozygotes. Clin. Chem. 51(4), 688–694 (2005).
  • Paschke E, Fauler G, Winkler H et al. Urinary total globotriaosylceramide and isoforms to identify women with Fabry disease: a diagnostic test study. Am. J. Kidney Dis. 57(5), 673–681 (2011).
  • Chatterjee S, Pandey A. The Yin and Yang of lactosylceramide metabolism: implications in cell function. Biochim. Biophys. Acta 1780(3), 370–382 (2008).
  • D’Angelo G, Uemura T, Chuang C-C et al. Vesicular and non-vesicular transport feed distinct glycosylation pathways in the Golgi. Nature 501(7465), 116–120 (2013).
  • Yamaji T, Nishikawa K, Hanada K. Transmembrane BAX Inhibitor Motif containing (TMBIM) family proteins perturbs a trans-Golgi network enzyme, Gb3 synthase, and reduces Gb3 biosynthesis. J. Biol. Chem. 285(46), 35505–35518 (2010).
  • Zhou H, Ma H, Wei W et al. B4GALT family mediates the multidrug resistance of human leukemia cells by regulating the hedgehog pathway and the expression of p-glycoprotein and multidrug resistance-associated protein 1. Cell Death Dis. 4, e654 (2013).
  • Liu Y-Y, Gupta V, Patwardhan GA et al. Glucosylceramide synthase upregulates MDR1 expression in the regulation of cancer drug resistance through cSrc and β-catenin signaling. Mol. Cancer 9, 145 (2010).
  • Gouaze-Andersson V, Cabot MC. Glycosphingolipids and drug resistance. Biochim. Biophys. Acta 1758(12), 2096–2103 (2006).
  • Gouazé V, Liu Y-Y, Prickett CS, Yu JY, Giuliano AE, Cabot MC. Glucosylceramide synthase blockade down-regulates P-glycoprotein and resensitizes multidrug-resistant breast cancer cells to anticancer drugs. Cancer Res. 65(9), 3861–3867 (2005).
  • Gouazé V, Yu JY, Bleicher RJ et al. Overexpression of glucosylceramide synthase and P-glycoprotein in cancer cells selected for resistance to natural product chemotherapy. Mol. Cancer Ther. 3(5), 633–639 (2004).
  • Veldman RJ, Sietsma H, Klappe K, Hoekstra D, Kok JW. Inhibition of P-glycoprotein activity and chemosensitization of multidrug-resistant ovarian carcinoma 2780AD cells by hexanoylglucosylceramide. Biochem. Biophys. Res. Commun. 266(2), 492–496 (1999).
  • Lucci A, Cho WI, Han TY, Giuliano AE, Morton DL, Cabot MC. Glucosylceramide: a marker for multiple-drug resistant cancers. Anticancer Res. 18(1B), 475–480 (1998).
  • Zhang X, Wu X, Li J et al. MDR1 (multidrug resistence 1) can regulate GCS (glucosylceramide synthase) in breast cancer cells. J. Surg. Oncol. 104(5), 466–471 (2011).
  • De Rosa MF. Inhibition of multidrug resistance by adamantylgb3, a globotriaosylceramide analog. J. Biol. Chem. 283(8), 4501 (2008).
  • Chai L, McLaren RP, Byrne A et al. The chemosensitizing activity of inhibitors of glucosylceramide synthase is mediated primarily through modulation of P-gp function. Int. J. Oncol. 38(3), 701–711 (2011).
  • Sakai K, Akiyama M, Sugiyama-Nakagiri Y, McMillan JR, Sawamura D, Shimizu H. Localization of ABCA12 from Golgi apparatus to lamellar granules in human upper epidermal keratinocytes. Exp. Dermatol. 16(11), 920–926 (2007).