Characterization and application of a disease-cell model for a neurodegenerative lysosomal disease

Molecular Genetics and Metabolism

Volumn 111, Issue 2, 2014, Pages 172-183

  Ribbens, Jameson J ^a   Moser, Ann B ^a   Hubbard, Walter C ^a   Bongarzone, Ernesto R ^b   Maegawa, Gustavo H B ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

Author keywords

Galactocerebrosidase; Globoid cell leukodystrophy; Krabbe disease; LC MS MS; Psychosine

Indexed keywords

CASPASE 3; CYCLOSERINE; CYTOCHROME C; GALACTOSYLCERAMIDASE; GALACTOSYLCERAMIDE; GLYCOSPHINGOLIPID; LYSOSOME ENZYME; PSYCHOSINE; VIRUS LARGE T ANTIGEN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPHAGY; CELL CULTURE; CELL IMMORTALIZATION; CELL LINE; CONTROLLED STUDY; CYTOSOL; DEGENERATIVE DISEASE; DEMYELINATION; ENZYME ACTIVATION; ENZYME RELEASE; GLIA CELL; GLOBOID CELL LEUKODYSTROPHY; LIPID HYDROLYSIS; LIQUID CHROMATOGRAPHY; LYSOSOME; LYSOSOME STORAGE DISEASE; MASS SPECTROMETRY; MOUSE; NONHUMAN; OLIGODENDROGLIA; PRIORITY JOURNAL; PROTEIN EXPRESSION; TWITCHER MOUSE;

MUS;

6-HEXADECANOYLAMINO-4-METHYLUMBELLIFERYL-Β-D-GALACTOSIDE; AC-DEDV-AMC; BEH; BRIDGED ETHYL HYBRID; GALACTOSYLCERAMIDE; GALC; GFAP; GLD; GLIAL FIBRILLARY ACIDIC PROTEIN; GLOBOID-CELL LEUKODYSTROPHY; HMUΒGAL; INTERNAL STANDARD; ISD; KRABBE DISEASE; LC-MS/MS; LSD; LYSOSOMAL STORAGE DISEASE; MAP-2; MASS SPECTROMETRY; MICROTUBULE-ASSOCIATED PROTEIN 2; MOBILE PHASE A; MOBILE PHASE B; MPA; MPB; MS; N-ACETYL-DEVD 7-AMIDO-4-METHYLCOUMARIN; PSYCHOSINE; RETENTION TIME; RT; SOLID-PHASE EXTRACTION; SPE; SV40-TRANFORMATION; SV40T; TWI; TWITCHER; Β-GALACTOCEREBROSIDASE;

ADULT; ANIMALS; ANTIGENS, POLYOMAVIRUS TRANSFORMING; AUTOPHAGY; BIOLOGICAL MARKERS; BRAIN; BRAIN CHEMISTRY; CASPASE 3; CELL LINE, TRANSFORMED; CYCLOSERINE; CYTOCHROMES C; FOUNDER EFFECT; GALACTOSYLCERAMIDASE; GALACTOSYLCERAMIDES; GENE EXPRESSION; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; INFANT; LEUKODYSTROPHY, GLOBOID CELL; MALE; MICE; MICROTUBULE-ASSOCIATED PROTEINS; MODELS, BIOLOGICAL; PSYCHOSINE;

EID: 84893677855     PISSN: 10967192     EISSN: 10967206     Source Type: Journal    
DOI: 10.1016/j.ymgme.2013.09.011     Document Type: Article

References (53)

1. Futerman A.H., Riezman H. The ins and outs of sphingolipid synthesis. Trends Cell Biol. 2005, 15:312-318.
2. Lee J.M., Lee Y.K., Mamrosh J.L., Busby S.A., Griffin P.R., Pathak M.C., Ortlund E.A., Moore D.D. A nuclear-receptor-dependent phosphatidylcholine pathway with antidiabetic effects. Nature 2011, 474:506-510.
3. Contreras F.X., Ernst A.M., Haberkant P., Bjorkholm P., Lindahl E., Gonen B., Tischer C., Elofsson A., von Heijne G., Thiele C., Pepperkok R., Wieland F., Brugger B. Molecular recognition of a single sphingolipid species by a protein's transmembrane domain. Nature 2012, 481:525-529.
4. Carette J.E., Raaben M., Wong A.C., Herbert A.S., Obernosterer G., Mulherkar N., Kuehne A.I., Kranzusch P.J., Griffin A.M., Ruthel G., Dal Cin P., Dye J.M., Whelan S.P., Chandran K., Brummelkamp T.R. Ebola virus entry requires the cholesterol transporter Niemann-Pick C1. Nature 2011, 477:340-343.
5. Petrache I., Natarajan V., Zhen L., Medler T.R., Richter A.T., Cho C., Hubbard W.C., Berdyshev E.V., Tuder R.M. Ceramide upregulation causes pulmonary cell apoptosis and emphysema-like disease in mice. Nat. Med. 2005, 11:491-498.
6. Fantini J., Yahi N. Molecular insights into amyloid regulation by membrane cholesterol and sphingolipids: common mechanisms in neurodegenerative diseases. Exp. Rev. Mol. Med. 2010, 12:e27.
7. Suzuki K. Twenty five years of the "psychosine hypothesis": a personal perspective of its history and present status. Neurochem. Res. 1998, 23:251-259.
8. Hawkins-Salsbury J.A., Parameswar A.R., Jiang X., Schelsinger P.H., Bongarzone E.R., Ory D.S., Demchenko A.V., Sands M.S. Psychosine, the cytotoxic sphingolipid that accumulates in globoid cell leukodystrophy, alters membrane architecture. J. Lipid Res. 2013 Sep 4, [Epub ahead of print].
9. Suzuki Y., Suzuki K. Krabbe's globoid cell leukodystrophy: deficiency of galactocerebrosidase in serum, leukocytes, and fibroblasts. Science 1971, 171:73-75.
10. Wenger D.A., Rafi M.A., Luzi P. Molecular genetics of Krabbe disease (globoid cell leukodystrophy): diagnostic and clinical implications. Hum. Mutat. 1997, 10:268-279.
11. Cleland W.W., Kennedy E.P. The enzymatic synthesis of psychosine. J. Biol. Chem. 1960, 235:45-51.
12. Miyatake T., Suzuki K. Globoid cell leukodystrophy: additional deficiency of psychosine galactosidase. Biochem. Biophys. Res. Commun. 1972, 48:539-543.
13. Taketomi T., Nishimura K. Physiological activity of psychosine. Jpn. J. Exp. Med. 1964, 34:255-265.
14. Igisu H., Suzuki K. Progressive accumulation of toxic metabolite in a genetic leukodystrophy. Science 1984, 224:753-755.
15. Chuang W.L., Pacheco J., Zhang X.K., Martin M.M., Biski C.K., Keutzer J.M., Wenger D.A., Caggana M., Orsini J.J. Determination of psychosine concentration in dried blood spots from newborns that were identified via newborn screening to be at risk for Krabbe disease. Clin. Chim. Acta 2013, 419:73-76.
16. Kobayashi T., Yamanaka T., Jacobs J.M., Teixeira F., Suzuki K. The Twitcher mouse: an enzymatically authentic model of human globoid cell leukodystrophy (Krabbe disease). Brain Res. 1980, 202:479-483.
17. Chatelut M., Harzer K., Christomanou H., Feunteun J., Pieraggi M.T., Paton B.C., Kishimoto Y., O'Brien J.S., Basile J.P., Thiers J.C., Salvayre R., Levade T. Model SV40-transformed fibroblast lines for metabolic studies of human prosaposin and acid ceramidase deficiencies. Clin. Chim. Acta 1997, 262:61-76.
18. Wiederschain G., Raghavan S., Kolodny E. Characterization of 6-hexadecanoylamino-4-methylumbelliferyl-beta-d-galactopyranoside as fluorogenic substrate of galactocerebrosidase for the diagnosis of Krabbe disease. Clin. Chim. Acta 1992, 205:87-96.
19. Nicholson D.W., Ali A., Thornberry N.A., Vaillancourt J.P., Ding C.K., Gallant M., Gareau Y., Griffin P.R., Labelle M., Lazebnik Y.A., et al. Identification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis. Nature 1995, 376:37-43.
20. Nestal de Moraes G., Carvalho E., Maia R.C., Sternberg C. Immunodetection of caspase-3 by Western blot using glutaraldehyde. Anal. Biochem. 2011, 415:203-205.
21. Kaneko T., Okita H., Nakajima H., Iijima K., Ogasawara N., Miyagawa Y., Katagiri Y.U., Nakagawa A., Kiyokawa N., Sato T., Fujimoto J. Neuroblastoma cells can be classified according to glycosphingolipid expression profiles identified by liquid chromatography-tandem mass spectrometry. Int. J. Oncol. 2010, 37:1279-1288.
22. Stahlman M., Ejsing C.S., Tarasov K., Perman J., Boren J., Ekroos K. High-throughput shotgun lipidomics by quadrupole time-of-flight mass spectrometry. J. Chromatogr. B Anal. Technol. Biomed. Life Sci. 2009, 877:2664-2672.
23. White A.B., Galbiati F., Givogri M.I., Lopez Rosas A., Qiu X., van Breemen R., Bongarzone E.R. Persistence of psychosine in brain lipid rafts is a limiting factor in the therapeutic recovery of a mouse model for Krabbe disease. J. Neurosci. Res. 2011, 89:352-364.
24. Sakai N., Inui K., Tatsumi N., Fukushima H., Nishigaki T., Taniike M., Nishimoto J., Tsukamoto H., Yanagihara I., Ozono K., Okada S. Molecular cloning and expression of cDNA for murine galactocerebrosidase and mutation analysis of the Twitcher mouse, a model of Krabbe's disease. J. Neurochem. 1996, 66:1118-1124.
25. Scherer M., Leuthauser-Jaschinski K., Ecker J., Schmitz G., Liebisch G. A rapid and quantitative LC-MS/MS method to profile sphingolipids. J. Lipid Res. 2010, 51:2001-2011.
26. Svennerholm L., Vanier M.T., Mansson J.E. Krabbe disease: a galactosylsphingosine (psychosine) lipidosis. J. Lipid Res. 1980, 21:53-64.
27. Li Y.T., Li S.C., Buck W.R., Haskins M.E., Wu S.W., Khoo K.H., Sidransky E., Bunnell B.A. Selective extraction and effective separation of galactosylsphingosine (psychosine) and glucosylsphingosine from other glycosphingolipids in pathological tissue samples. Neurochem. Res. 2011, 36:1612-1622.
28. Schueler U.H., Kolter T., Kaneski C.R., Blusztajn J.K., Herkenham M., Sandhoff K., Brady R.O. 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, 14:595-601.
29. He C., Klionsky D.J. Regulation mechanisms and signaling pathways of autophagy. Annu. Rev. Genet. 2009, 43:67-93.
30. Settembre C., Fraldi A., Rubinsztein D.C., Ballabio A. Lysosomal storage diseases as disorders of autophagy. Autophagy 2008, 4:113-114.
31. Klionsky D.J., Abeliovich H., Agostinis P., Agrawal D.K., Aliev G., Askew D.S., Baba M., Baehrecke E.H., Bahr B.A., Ballabio A., Bamber B.A., Bassham D.C., Bergamini E., Bi X., Biard-Piechaczyk M., Blum J.S., Bredesen D.E., Brodsky J.L., Brumell J.H., Brunk U.T., Bursch W., Camougrand N., Cebollero E., Cecconi F., Chen Y., Chin L.S., Choi A., Chu C.T., Chung J., Clarke P.G., Clark R.S., Clarke S.G., Clave C., Cleveland J.L., Codogno P., Colombo M.I., Coto-Montes A., Cregg J.M., Cuervo A.M., Debnath J., Demarchi F., Dennis P.B., Dennis P.A., Deretic V., Devenish R.J., Di Sano F., Dice J.F., Difiglia M., Dinesh-Kumar S., Distelhorst C.W., Djavaheri-Mergny M., Dorsey F.C., Droge W., Dron M., Dunn W.A., Duszenko M., Eissa N.T., Elazar Z., Esclatine A., Eskelinen E.L., Fesus L., Finley K.D., Fuentes J.M., Fueyo J., Fujisaki K., Galliot B., Gao F.B., Gewirtz D.A., Gibson S.B., Gohla A., Goldberg A.L., Gonzalez R., Gonzalez-Estevez C., Gorski S., Gottlieb R.A., Haussinger D., He Y.W., Heidenreich K., Hill J.A., Hoyer-Hansen M., Hu X., Huang W.P., Iwasaki A., Jaattela M., Jackson W.T., Jiang X., Jin S., Johansen T., Jung J.U., Kadowaki M., Kang C., Kelekar A., Kessel D.H., Kiel J.A., Kim H.P., Kimchi A., Kinsella T.J., Kiselyov K., Kitamoto K., Knecht E., Komatsu M., Kominami E., Kondo S., Kovacs A.L., Kroemer G., Kuan C.Y., Kumar R., Kundu M., Landry J., Laporte M., Le W., Lei H.Y., Lenardo M.J., Levine B., Lieberman A., Lim K.L., Lin F.C., Liou W., Liu L.F., Lopez-Berestein G., Lopez-Otin C., Lu B., Macleod K.F., Malorni W., Martinet W., Matsuoka K., Mautner J., Meijer A.J., Melendez A., Michels P., Miotto G., Mistiaen W.P., Mizushima N., Mograbi B., Monastyrska I., Moore M.N., Moreira P.I., Moriyasu Y., Motyl T., Munz C., Murphy L.O., Naqvi N.I., Neufeld T.P., Nishino I., Nixon R.A., Noda T., Nurnberg B., Ogawa M., Oleinick N.L., Olsen L.J., Ozpolat B., Paglin S., Palmer G.E., Papassideri I., Parkes M., Perlmutter D.H., Perry G., Piacentini M., Pinkas-Kramarski R., Prescott M., Proikas-Cezanne T., Raben N., Rami A., Reggiori F., Rohrer B., Rubinsztein D.C., Ryan K.M., Sadoshima J., Sakagami H., Sakai Y., Sandri M., Sasakawa C., Sass M., Schneider C., Seglen P.O., Seleverstov O., Settleman J., Shacka J.J., Shapiro I.M., Sibirny A., Silva-Zacarin E.C., Simon H.U., Simone C., Simonsen A., Smith M.A., Spanel-Borowski K., Srinivas V., Steeves M., Stenmark H., Stromhaug P.E., Subauste C.S., Sugimoto S., Sulzer D., Suzuki T., Swanson M.S., Tabas I., Takeshita F., Talbot N.J., Talloczy Z., Tanaka K., Tanida I., Taylor G.S., Taylor J.P., Terman A., Tettamanti G., Thompson C.B., Thumm M., Tolkovsky A.M., Tooze S.A., Truant R., Tumanovska L.V., Uchiyama Y., Ueno T., Uzcategui N.L., van der Klei I., Vaquero E.C., Vellai T., Vogel M.W., Wang H.G., Webster P., Wiley J.W., Xi Z., Xiao G., Yahalom J., Yang J.M., Yap G., Yin X.M., Yoshimori T., Yu L., Yue Z., Yuzaki M., Zabirnyk O., Zheng X., Zhu X., Deter R.L. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008, 4:151-175.
32. Mellors J.S., Jorgenson J.W. Use of 1.5-microm porous ethyl-bridged hybrid particles as a stationary-phase support for reversed-phase ultrahigh-pressure liquid chromatography. Anal. Chem. 2004, 76:5441-5450.
33. Sittampalam G., Gal-Edd N., Weidner J., Auld D., Glicksman M., Arkin M., Napper A., Inglese J. Assay Guidance Manual 2004, Eli Lilly & Company and the National Center for Advancing Translational Sciences, Bethesda, MD.
34. LeVine S.M., Pedchenko T.V., Bronshteyn I.G., Pinson D.M. l-Cycloserine slows the clinical and pathological course in mice with globoid cell leukodystrophy (Twitcher mice). J. Neurosci. Res. 2000, 60:231-236.
35. Suzuki K. Globoid cell leukodystrophy (Krabbe's disease): update. J. Child Neurol. 2003, 18:595-603.
36. Grabowski G.A., Hopkin R.J. Enzyme therapy for lysosomal storage disease: principles, practice, and prospects. Annu. Rev. Genomics Hum. Genet. 2003, 4:403-436.
37. Biswas S., LeVine S.M. Substrate-reduction therapy enhances the benefits of bone marrow transplantation in young mice with globoid cell leukodystrophy. Pediatr. Res. 2002, 51:40-47.
38. Escolar M.L., Poe M.D., Provenzale J.M., Richards K.C., Allison J., Wood S., Wenger D.A., Pietryga D., Wall D., Champagne M., Morse R., Krivit W., Kurtzberg J. Transplantation of umbilical-cord blood in babies with infantile Krabbe's disease. N. Engl. J. Med. 2005, 352:2069-2081.
39. Duffner P.K., Caviness V.S., Erbe R.W., Patterson M.C., Schultz K.R., Wenger D.A., Whitley C. The long-term outcomes of presymptomatic infants transplanted for Krabbe disease: report of the workshop held on July 11 and 12, 2008, Holiday Valley, New York. Genet. Med. 2009, 11:450-454.
40. Duffner P.K., Caggana M., Orsini J.J., Wenger D.A., Patterson M.C., Crosley C.J., Kurtzberg J., Arnold G.L., Escolar M.L., Adams D.J., Andriola M.R., Aron A.M., Ciafaloni E., Djukic A., Erbe R.W., Galvin-Parton P., Helton L.E., Kolodny E.H., Kosofsky B.E., Kronn D.F., Kwon J.M., Levy P.A., Miller-Horn J., Naidich T.P., Pellegrino J.E., Provenzale J.M., Rothman S.J., Wasserstein M.P. Newborn screening for Krabbe disease: the New York State model. Pediatr. Neurol. 2009, 40:245-252. (discussion 253-245).
41. Buntinx M., Vanderlocht J., Hellings N., Vandenabeele F., Lambrichts I., Raus J., Ameloot M., Stinissen P., Steels P., Buntinx M., Vanderlocht J., Hellings N., Vandenabeele F., Lambrichts I., Raus J., Ameloot M., Stinissen P., Steels P. Characterization of three human oligodendroglial cell lines as a model to study oligodendrocyte injury: morphology and oligodendrocyte-specific gene expression. J. Neurocytol. 2003, 32:25-38.
42. Bongarzone E.R., Foster L.M., Byravan S., Schonmann V., Campagnoni A.T. Temperature-dependent regulation of PLP/DM20 and CNP gene expression in two conditionally-immortalized jimpy oligodendrocyte cell lines. Neurochem. Res. 1997, 22:363-372.
43. Verity A.N., Bredesen D., Vonderscher C., Handley V.W., Campagnoni A.T. Expression of myelin protein genes and other myelin components in an oligodendrocytic cell line conditionally immortalized with a temperature-sensitive retrovirus. J. Neurochem. 1993, 60:577-587.
44. Feutz A.C., Bellomi I., Allinquant B., Schladenhaufen Y., Ghandour M.S. Isolation and characterization of defective jimpy oligodendrocytes in culture. J. Neurocytol. 1995, 24:865-877.
45. Feutz A.C., Pham-Dinh D., Allinquant B., Miehe M., Ghandour M.S. An immortalized jimpy oligodendrocyte cell line: defects in cell cycle and cAMP pathway. Glia 2001, 34:241-252.
46. Baarine M., Ragot K., Genin E.C., El Hajj H., Trompier D., Andreoletti P., Ghandour M.S., Menetrier F., Cherkaoui-Malki M., Savary S., Lizard G. Peroxisomal and mitochondrial status of two murine oligodendrocytic cell lines (158N, 158JP): potential models for the study of peroxisomal disorders associated with dysmyelination processes. J. Neurochem. 2009, 111:119-131.
47. Shen J.S., Watabe K., Meng X.L., Ida H., Ohashi T., Eto Y. Establishment and characterization of spontaneously immortalized Schwann cells from murine model of globoid cell leukodystrophy (twitcher). J. Neurosci. Res. 2002, 68:588-594.
48. Yim S.H., Szuchet S., Polak P.E. Cultured oligodendrocytes A role for cell-substratum interaction in phenotypic expression. J. Biol. Chem. 1986, 261:11808-11815.
49. Zaka M., Wenger D.A. Psychosine-induced apoptosis in a mouse oligodendrocyte progenitor cell line is mediated by caspase activation. Neurosci. Lett. 2004, 358:205-209.
50. Giri S., Khan M., Rattan R., Singh I., Singh A.K. Krabbe disease: psychosine-mediated activation of phospholipase A2 in oligodendrocyte cell death. J. Lipid Res. 2006, 47:1478-1492.
51. Suen D.F., Norris K.L., Youle R.J. Mitochondrial dynamics and apoptosis. Genes Dev. 2008, 22:1577-1590.
52. Vitner E.B., Platt F.M., Futerman A.H. Common and uncommon pathogenic cascades in lysosomal storage diseases. J. Biol. Chem. 2010, 285:20423-20427.
53. Lam M.P., Scruggs S.B., Kim T.Y., Zong C., Lau E., Wang D., Ryan C.M., Faull K.F., Ping P. An MRM-based workflow for quantifying cardiac mitochondrial protein phosphorylation in murine and human tissue. J. Proteome 2012, 75:4602-4609.