journal article Jan 31, 2014

High sphingomyelin levels induce lysosomal damage and autophagy dysfunction in Niemann Pick disease type A

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References
45
[1]
Platt FM, Boland B, van der Spoel AC . The cell biology of disease: lysosomal storage disorders: the cellular impact of lysosomal dysfunction. J Cell Biol 2012; 199: 723–734. 10.1083/jcb.201208152
[2]
Lieberman AP, Puertollano R, Raben N, Slaugenhaupt S, Walkley SU, Ballabio A . Autophagy in lysosomal storage disorders. Autophagy 2012; 8: 719–730. 10.4161/auto.19469
[3]
Autophagy fights disease through cellular self-digestion

Noboru Mizushima, Beth Levine, Ana Maria Cuervo et al.

Nature 2008 10.1038/nature06639
[4]
Boya P, Reggiori F, Codogno P . Emerging regulation and functions of autophagy. Nat Cell Biol 2013; 15: 713–720. 10.1038/ncb2788
[5]
Brady RO, Kanfer JN, Mock MB, Fredrickson DS . The metabolism of sphingomyelin. II. Evidence of an enzymatic deficiency in Niemann-Pick diseae. Proc Natl Acad Sci USA 1966; 55: 366–369. 10.1073/pnas.55.2.366
[6]
Stoffel W . Functional analysis of acid and neutral sphingomyelinases in vitro and in vivo. Chem Phys Lipids 1999; 102: 107–121. 10.1016/s0009-3084(99)00079-1
[7]
Ledesma MD, Prinetti A, Sonnino S, Schuchman EH . Brain pathology in Niemann Pick disease type A: insights from the acid sphingomyelinase knockout mice. J Neurochem 2011; 116: 779–788. 10.1111/j.1471-4159.2010.07034.x
[8]
Schuchman EH . The pathogenesis and treatment of acid sphingomyelinase-deficient Niemann-Pick disease. Int J Clin Pharmacol Ther 2009; 47 (Suppl 1): S48–S57.
[9]
Horinouchi K, Erlich S, Perl DP, Ferlinz K, Bisgaier CL, Sandhoff K et al. Acid sphingomyelinase deficient mice: a model of types A and B Niemann-Pick disease. Nat. Genet 1995; 10: 288–293. 10.1038/ng0795-288
[10]
Galvan C, Camoletto PG, Cristofani F, Van Veldhoven PP, Ledesma MD . Anomalous surface distribution of glycosyl phosphatidyl inositol-anchored proteins in neurons lacking acid sphingomyelinase. Mol Biol Cell 2008; 19: 509–522. 10.1091/mbc.e07-05-0439
[11]
Camoletto PG, Vara H, Morando L, Connell E, Marletto FP, Giustetto M et al. Synaptic vesicle docking: sphingosine regulates syntaxin1 interaction with Munc18. PLoS One 2009; 4: e5310. 10.1371/journal.pone.0005310
[12]
Macauley SL, Sidman RL, Schuchman EH, Taksir T, Stewart GR . Neuropathology of the acid sphingomyelinase knockout mouse model of Niemann-Pick A disease including structure-function studies associated with cerebellar Purkinje cell degeneration. Exp Neurol 2008; 214: 181–192. 10.1016/j.expneurol.2008.07.026
[13]
Korolchuk VI, Mansilla A, Menzies FM, Rubinsztein DC . Autophagy inhibition compromises degradation of ubiquitin-proteasome pathway substrates. Mol Cell 2009; 33: 517–527. 10.1016/j.molcel.2009.01.021
[14]
Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I et al. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 2006; 441: 880–884. 10.1038/nature04723
[15]
Pankiv S, Clausen TH, Lamark T, Brech A, Bruun JA, Outzen H et al. p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. J Biol Chem 2007; 282: 24131–24145. 10.1074/jbc.m702824200
[16]
Kirkin V, Lamark T, Sou YS, Bjørkøy G, Nunn JL, Bruun JA et al. A role for NBR1 in autophagosomal degradation of ubiquitinated substrates. Mol Cell 2009; 33: 505–516. 10.1016/j.molcel.2009.01.020
[17]
Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice

Taichi Hara, Kenji Nakamura, Makoto Matsui et al.

Nature 2006 10.1038/nature04724
[18]
Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I et al. Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 2006; 441: 880–884. 10.1038/nature04723
[19]
Suurmeijer AJ, van der Wijk J, van Veldhuisen DJ, Yang F, Cole GM . Fractin immunostaining for the detection of apoptotic cells and apoptotic bodies in formalin-fixed and paraffin-embedded tissue. Lab Invest 1999; 79: 619–620.
[20]
Dall’Armi C, Devereaux KA, Di Paolo G . The role of lipids in the control of autophagy. Curr Biol 2013; 23: R33–R45. 10.1016/j.cub.2012.10.041
[21]
Fraldi A, Annunziata F, Lombardi A, Kaiser HJ, Medina DL, Spampanato C et al. Lysosomal fusion and SNARE function are impaired by cholesterol accumulation in lysosomal storage disorders. EMBO J 2010; 29: 3607–3620. 10.1038/emboj.2010.237
[22]
Elrick MJ, Yu T, Chung C, Lieberman AP . Impaired proteolysis underlies autophagic dysfunction in Niemann-Pick type C disease. Hum Mol Genet 2012; 21: 4876–4887. 10.1093/hmg/dds324
[23]
Tamboli IY, Hampel H, Tien NT, Tolksdorf K, Breiden B, Mathews PM et al. Sphingolipid storage affects autophagic metabolism of the amyloid precursor protein and promotes Abeta generation. J Neurosci 2011; 31: 1837–1849. 10.1523/jneurosci.2954-10.2011
[24]
Sarkar S, Carroll B, Buganim Y, Maetzel D, Ng AH, Cassady JP et al. Impaired autophagy in the lipid-storage disorder Niemann-pick type C1 disease. Cell Rep 2013; 5: 1302–1315. 10.1016/j.celrep.2013.10.042
[25]
Kiyokawa E, Makino A, Ishii K, Otsuka N, Yamaji-Hasegawa A, Kobayashi T . Recognition of sphingomyelin by lysenin and lysenin-related proteins. Biochemistry 2004; 43: 9766–9773. 10.1021/bi049561j
[26]
Haglund K, Dikic I . The role of ubiquitylation in receptor endocytosis and endosomal sorting. J Cell Sci 2012; 125: 265–275. 10.1242/jcs.091280
[27]
Ravikumar B, Moreau K, Jahreiss L, Puri C, Rubinsztein DC . Plasma membrane contributes to the formation of pre-autophagosomal structures. Nat Cell Biol 2010; 12: 747–757. 10.1038/ncb2078
[28]
Ramachandran CK, Murray DK, Nelson DH . Dexamethasone increases neutral sphingomyelinase activity and sphingosine levels in 3T3-L1 fibroblasts. Biochem Biophys Res Commun 1990; 167: 607–613. 10.1016/0006-291x(90)92068-b
[29]
Shihabuddin LS, Numan S, Huff MR, Dodge JC, Clarke J, Macauley SL et al. Intracerebral transplantation of adult mouse neural progenitor cells into the Niemann-Pick-A mouse leads to a marked decrease in lysosomal storage pathology. J Neurosci 2004; 24: 10642–10651. 10.1523/jneurosci.3584-04.2004
[30]
Passini MA, Macauley SL, Huff MR, Taksir TV, Bu J, Wu IH et al. AAV vector-mediated correction of brain pathology in a mouse model of Niemann-Pick A disease. Mol Ther 2005; 11: 754–762. 10.1016/j.ymthe.2005.01.011
[31]
Jablin MS, Flasiński M, Dubey M, Ratnaweera DR, Broniatowski M, Dynarowicz-Łatka P et al. Effects of beta-cyclodextrin on the structure of sphingomyelin/cholesterol model membranes. Biophys J 2010; 99: 1475–1481. 10.1016/j.bpj.2010.06.028
[32]
Dissection of the Autophagosome Maturation Process by a Novel Reporter Protein, Tandem Fluorescent-Tagged LC3

Shunsuke Kimura, Takeshi Noda, Tamotsu Yoshimori

Autophagy 2007 10.4161/auto.4451
[33]
Reiser J, Adair B, Reinheckel T . Specialized roles for cysteine cathepsins in health and disease. J Clin Invest 2010; 120: 3421–3431. 10.1172/jci42918
[34]
Moles A, Tarrats N, Fernández-Checa JC, Marí M . Cathepsin B overexpression due to acid sphingomyelinase ablation promotes liver fibrosis in Niemann-Pick disease. J Biol Chem 2012; 287: 1178–1188. 10.1074/jbc.m111.272393
[35]
Boya P, Kroemer G . Lysosomal membrane permeabilization in cell death. Oncogene 2008; 27: 6434–6451. 10.1038/onc.2008.310
[36]
Kirkegaard T, Roth AG, Petersen NH, Mahalka AK, Olsen OD, Moilanen I et al. Hsp70 stabilizes lysosomes and reverts Niemann-Pick disease-associated lysosomal pathology. Nature 2010; 463: 549–553. 10.1038/nature08710
[37]
Nylandsted J, Gyrd-Hansen M, Danielewicz A, Fehrenbacher N, Lademann U, Høyer-Hansen M et al. Heat shock protein 70 promotes cell survival by inhibiting lysosomal membrane permeabilization. J Exp Med 2004; 200: 425–435. 10.1084/jem.20040531
[38]
Boya P . Lysosomal function and dysfunction: mechanism and disease. Antioxid Redox Signal. 2012; 17: 766–774. 10.1089/ars.2011.4405
[39]
Settembre C, Fraldi A, Jahreiss L, Spampanato C, Venturi C, Medina D et al. A block of autophagy in lysosomal storage disorders. Hum Mol Genet 2008; 17: 119–129. 10.1093/hmg/ddm289
[40]
Pacheco CD, Kunkel R, Lieberman AP . Autophagy in Niemann-Pick C disease is dependent upon Beclin-1 and responsive to lipid trafficking defects. Hum Mol Genet 2007; 16: 1495–1503. 10.1093/hmg/ddm100
[41]
Liou W, Geuze HJ, Geelen MJ, Slot JW . The autophagic and endocytic pathways converge at the nascent autophagic vacuoles. J Cell Biol 1997; 136: 61–70. 10.1083/jcb.136.1.61
[42]
Lucocq J, Walker D . Evidence for fusion between multilamellar endosomes and autophagosomes in HeLa cells. Eur J Cell Biol 1997; 72: 307–313.
[43]
Puri C, Renna M, Bento CF, Moreau K, Rubinsztein DC . Diverse autophagosome membrane sources coalesce in recycling endosomes. Cell 2013; 154: 1285–1299. 10.1016/j.cell.2013.08.044
[44]
Moreau K, Ravikumar B, Renna M, Puri C, Rubinsztein DC . Autophagosome precursor maturation requires homotypic fusion. Cell 2011; 146: 303–317. 10.1016/j.cell.2011.06.023
[45]
Dotti CG, Sullivan CA, Banker GA . The establishment of polarity by hippocampal neurons in culture. J Neurosci 1988; 8: 1454–1468. 10.1523/jneurosci.08-04-01454.1988
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Published
Jan 31, 2014
Vol/Issue
21(6)
Pages
864-875
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Cite This Article
E Gabandé-Rodríguez, P Boya, V Labrador, et al. (2014). High sphingomyelin levels induce lysosomal damage and autophagy dysfunction in Niemann Pick disease type A. Cell Death & Differentiation, 21(6), 864-875. https://doi.org/10.1038/cdd.2014.4
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