Cholesterol accumulation is associated with lysosomal dysfunction and autophagic stress in Npc1-/- mouse brain

American Journal of Pathology

Volumn 171, Issue 3, 2007, Pages 962-975

  Liao, Guanghong ^a   Yao, Yueqin ^b   Liu, Jihua ^b   Yu, Zhang ^c   Cheung, Simon ^a   Xie, Ang ^a   Liang, Xiaoli ^d   Bi, Xiaoning ^a  

^a WESTERN UNIVERSITY OF HEALTH SCIENCES   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c FUDAN UNIVERSITY   (China)

^d Beijing Military Medical College   (China)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN ENZYME; CATHEPSIN D; CHOLESTEROL; FILIPIN; LYSOSOME ENZYME;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; AUTOPHAGY; BRAIN; CELL FUNCTION; CELL STRUCTURE; CELL VACUOLE; ELECTRON MICROSCOPY; ENDOSOME; FEMALE; IMMUNOBLOTTING; IMMUNOFLUORESCENCE TEST; LYSOSOME; MALE; MICROGLIA; MOUSE; MUTANT; NERVE CELL; NERVE DEGENERATION; NONHUMAN; POSTNATAL DEVELOPMENT; PRIORITY JOURNAL; PURKINJE CELL; WILD TYPE;

EID: 34548860918     PISSN: 00029440     EISSN: None     Source Type: Journal    
DOI: 10.2353/ajpath.2007.070052     Document Type: Article

References (72)

1. Vance JE: Lipid imbalance in the neurological disorder, Niemann-Pick C disease. FEBS Lett 2006, 580:5518-5524
2. Chang TY, Reid PC, Sugii S, Ohgami N, Cruz JC, Chang CC: Niemann-Pick type C disease and intracellular cholesterol trafficking. J Biol Chem 2005, 280:20917-20920
3. Carstea ED, Morris JA, Coleman KG, Loftus SK, Zhang D, Cummings C, Gu J, Rosenfeld MA, Pavan WJ, Krizman DB, Nagle J, Polymeropoulos MH, Sturley SL, Ioannou YA, Higgins ME, Comly M, Cooney A, Brown A, Kaneski CR, Blanchette-Mackie EJ, Dwyer NK, Neufeld EB, Chang TY, Liscum L, Strauss JF, Ohno K, Zeigler M, Carmi R, Sokol J, Markie D, O'Neill RR, van Diggelen OP, Elleder M, Patterson MC, Brady RO, Vanier MT, Pentchev PG Tagle DA: Niemann-Pick C1 disease gene: homology to mediators of cholesterol homeostasis. Science 1997, 277:228-231
4. Blom TS, Linder MD, Snow K, Pinko H, Hess MW, Jokitalo E, Veckman V, Syvanen AC, Ikonen E: Defective endocytic trafficking of NPC1 and NPC2 underlying infantile Niemann-Pick type C disease. Hum Mol Genet 2003, 12:257-272
5. Garver WS, Heidenreich RA: The Niemann-Pick C proteins and trafficking of cholesterol through the late endosomal/lysosomal system. Curr Mol Med 2002, 2:485-505
6. Ory DS: Niemann-Pick type C: a disorder of cellular cholesterol trafficking. Biochim Biophys Acta 2000, 1529:331-339
7. Burns M, Duff K: Cholesterol in Alzheimer's disease and tauopathy. Ann NY Acad Sci 2002, 977:367-375
8. Liscum L: Niemann-Pick type C mutations cause lipid traffic jam. Traffic 2000, 1:218-225
9. Strittmatter WJ: Apolipoprotein E and Alzheimer's disease. Ann NY Acad Sci 2000, 924:91-92
10. Michikawa M: Cholesterol paradox: is high total or low HDL cholesterol level a risk for Alzheimer's disease? J Neurosci Res 2003, 72:141-146
11. Nixon RA, Cataldo AM, Mathews PM: The endosomal-lysosomal system of neurons in Alzheimer's disease pathogenesis: a review. Neurochem Res 2000, 25:1161-1172
12. Auer IA, Schmidt ML, Lee VM, Curry B, Suzuki K, Shin RW, Pentchev PG, Carstea ED, Trojanowski JQ: Paired helical filament tau (PHFtau) in Niemann-Pick type C disease is similar to PHFtau in Alzheimer's disease. Acta Neuropathol (Berl) 1995, 90:547-551
13. Suzuki K, Parker CC, Pentchev PG, Katz D, Ghetti B, D'Agostino AN, Carstea ED: Neurofibrillary tangles in Niemann-Pick disease type C. Acta Neuropathol (Berl) 1995, 89:227-238
14. Love S, Bridges LR, Case CP: Neurofibrillary tangles in Niemann-Pick disease type C. Brain 1995, 118:119-129
15. Patterson MC, Pentchev PG: Niemann-Pick; type C. Neurology 1996, 46:1785-1786
16. Distl R, Meske V, Ohm TG: Tangle-bearing neurons contain more free cholesterol than adjacent tangle-free neurons. Acta Neuropathol (Berl) 2001, 101:547-554
17. Distl R, Treiber-Held S, Albert F, Meske V, Harzer K, Ohm TG: Cholesterol storage and tau pathology in Niemann-Pick type C disease in the brain. J Pathol 2003, 200:104-111
18. Cataldo AM, Paskevich PA, Kominami E, Nixon RA: Lysosomal hydrolases of different classes are abnormally distributed in brains of patients with Alzheimer disease. Proc Natl Acad Sci USA 1991, 88:10998-11002
19. Ginsberg SD, Hemby SE, Lee VM, Eberwine JH, Trojanowski JQ: Expression profile of transcripts in Alzheimer's disease tangle-bearing CA1 neurons. Ann Neurol 2000, 48:77-87
20. Callahan LM, Vaules WA, Coleman PD: Quantitative decrease in synaptophysin message expression and increase in cathepsin D message expression in Alzheimer disease neurons containing neurofibrillary tangles. J Neuropathol Exp Neurol 1999, 58:275-287
21. Bi X, Yong AP, Zhou J, Ribak CE, Lynch G: Rapid induction of intraneuronal neurofibrillary tangles in apolipoprotein E-deficient mice. Proc Natl Acad Sci USA 2001, 98:8832-8837
22. Bidère N, Lorenzo HK, Carmona S, Laforge M, Harper F, Dumont C, Senik A: Cathepsin D triggers Bax activation, resulting in selective apoptosis-inducing factor (AIF) relocation in T lymphocytes entering the early commitment phase to apoptosis. J Biol Chem 2003, 278:31401-31411
23. Johansson AC, Steen H, Ollinger K, Roberg K: Cathepsin D mediates cytochrome c release and caspase activation in human fibroblast apoptosis induced by staurosporine. Cell Death Differ 2003, 10:1253-1259
24. Cirman T, Oresic K, Mazovec GD, Turk V, Reed JC, Myers RM, Salvesen GS, Turk B: Selective disruption of lysosomes in HeLa cells triggers apoptosis mediated by cleavage of Bid by multiple papain-like lysosomal cathepsins. J Biol Chem 2004, 279:3578-3587
25. Schweichel JU, Merker HJ: The morphology of various types of cell death in prenatal tissues. Teratology 1973, 7:253-266
26. Uchiyama Y: Autophagic cell death and its execution by lysosomal cathepsins. Arch Histol Cytol 2001, 64:233-246
27. Clarke PG: Developmental cell death: morphological diversity and multiple mechanisms. Anat Embryol (Berl) 1990, 181:195-213
28. Stadelmann C, Deckwerth TL, Srinivasan A, Bancher C, Bruck W, Jellinger K, Lassmann H: Activation of caspase-3 in single neurons and autophagic granules of granulovacuolar degeneration in Alzheimer's disease: evidence for apoptotic cell death. Am J Pathol 1999, 155:1459-1466
29. Nixon RA, Wegiel J, Kumar A, Yu WH, Peterhoff C, Cataldo A, Cuervo AM: Extensive involvement of autophagy in Alzheimer disease: an immuno-electron microscopy study. J Neuropathol Exp Neurol 2005, 64:113-122
30. Anglade P, Vyas S, Javoy-Agid F, Herrero MT, Michel PP, Marquez J, Mouatt-Prigent A, Ruberg M, Hirsch EC, Agid Y: Apoptosis and autophagy in nigral neurons of patients with Parkinson's disease. Histol Histopathol 1997, 12:25-31
31. Ko DC, Milenkovic L, Beier SM, Manuel H, Buchanan J, Scott MP: Cell-autonomous death of cerebellar Purkinje neurons with autophagy in Niemann-Pick type C disease. PLoS Genet 2005, 1:81-95
32. Baudry M, Yao Y, Simmons D, Liu J, Bi X: Postnatal development of inflammation in a murine model of Niemann-Pick type C disease: immunohistochemical observations of microglia and astroglia. Exp Neurol 2003, 184:887-903
33. Kabeya Y, Mizushima N, Ueno T, Yamamoto A, Kirisako T, Noda T, Kominami E, Ohsumi Y, Yoshimori T: LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 2000, 19:5720-5728
34. Bornig H, Geyer G: Staining of cholesterol with the fluorescent antibiotic "filipin." Acta Histochem 1974, 50:110-115
35. Bednarski E, Ribak CE, Lynch G: Suppression of cathepsins B and L causes a proliferation of lysosomes and the formation of meganeurites in hippocampus. J Neurosci 1997, 17:4006-4021
36. Liaudet-Coopman E, Beaujouin M, Derocq D, Garcia M, Glondu-Lassis M, Laurent-Matha V, Prebois C, Rochefort H, Vignon F: Cathepsin D: Newly discovered functions of a long-standing aspartic protease in cancer and apoptosis. Cancer Lett 2006, 237:167-179
37. Folio C, Castino R, Nicotra G, Trincheri NF, Isidoro C: Folding, activity and targeting of mutated human cathepsin D that cannot be processed into the double-chain form. Int J Biochem Cell Biol 2007, 39:638-649
38. Jäger S, Bucci C, Tanida I, Ueno T, Kominami E, Saftig P, Eskelinen EL: Role for Rab7 in maturation of late autophagic vacuoles. J Cell Sci 2004, 117:4837-4848
39. Gutierrez MG, Munafo DB, Beron W, Colombo MI: Rab7 is required for the normal progression of the autophagic pathway in mammalian cells. J Cell Sci 2004, 117:2687-2697
40. Mariño G, Lopez-Otin C: Autophagy: molecular mechanisms, physiological functions and relevance in human pathology. Cell Mol Life Sci 2004, 61:1439-1454
41. Keller JN, Dimayuga E, Chen Q, Thorpe J, Gee J, Ding Q: Autophagy, proteasomes, lipofuscin, and oxidative stress in the aging brain. Int J Biochem Cell Biol 2004, 36:2376-2391
42. Tanida I, Tanida-Miyake E, Ueno T, Kominami E: The human homolog of Saccharomyces cerevisiae Apg7p is a protein-activating enzyme for multiple substrates including human Apg12p, GATE-16, GABARAP, and MAP-LC3. J Biol Chem 2001, 276:1701-1706
43. Gozuacik D, Kimchi A: Autophagy as a cell death and tumor suppressor mechanism. Oncogene 2004, 23:2891-2906
44. German DC, Liang CL, Song T, Yazdani U, Xie C, Dietschy JM: Neurodegeneration in the Niemann-Pick C mouse: glial involvement. Neuroscience 2002, 109:437-450
45. Lynch G, Bi X: Lysosomes and brain aging in mammals. Neurochem Res 2003, 28:1725-1734
46. Bi X, Haque TS, Zhou J, Skillman AG, Lin B, Lee CE, Kuntz ID, Ellman JA, Lynch G: Novel cathepsin D inhibitors block the formation of hyperphosphorylated tau fragments in hippocampus. J Neurochem 2000, 74:1469-1477
47. Bednarski E, Lynch G: Cytosolic proteolysis of tau by cathepsin D in hippocampus following suppression of cathepsins B and L. J Neurochem 1996, 67:1846-1855
48. Bi X, Zhou J, Lynch G: Lysosomal protease inhibitors induce meganeurites and tangle-like structures in entorhinohippocampal regions vulnerable to Alzheimer's disease. Exp Neurol 1999, 158:312-327
49. Yang AJ, Chandswangbhuvana D, Margol L, Glabe CG: Loss of endosomal/lysosomal membrane impermeability is an early event in amyloid Aβ1-42 pathogenesis. J Neurosci Res 1998, 52:691-698
50. Burns M, Gaynor K, Olm V, Mercken M, LaFrancois J, Wang L, Mathews PM, Noble W, Matsuoka Y, Duff K: Presenilin redistribution associated with aberrant cholesterol transport enhances β-amyloid production in vivo. J Neurosci 2003, 23:5645-5649
51. Pagano RE: Endocytic trafficking of glycosphingolipids in sphingolipid storage diseases. Philos Trans R Soc Lond B Biol Sci 2003, 358:885-891
52. Lebrand C, Corti M, Goodson H, Cosson P, Cavalli V, Mayran N, Faure J, Gruenberg J: Late endosome motility depends on lipids via the small GTPase Rab7. EMBO J 2002, 21:1289-1300
53. Choudhury A, Dominguez M, Puri V, Sharma DK, Narita K, Wheatley CL, Marks DL, Pagano RE: Rab proteins mediate Golgi transport of caveola-internalized glycosphingolipids and correct lipid trafficking in Niemann-Pick C cells. J Clin Invest 2002, 109:1541-1550
54. Mayran N, Parton RG, Gruenberg J: Annexin II regulates multivesicular endosome biogenesis in the degradation pathway of animal cells. EMBO J 2003, 22:3242-3253
55. -/- mouse brain. Am J Pathol 2005, 167:1081-1092
56. Bijur GN, Jope RS: Glycogen synthase kinase-3β is highly activated in nuclei and mitochondria. Neuroreport 2003, 14:2415-2419
57. Zhu JH, Guo F, Shelburne J, Watkins S, Chu CT: Localization of phosphorylated ERK/MAP kinases to mitochondria and autophagosomes in Lewy body diseases. Brain Pathol 2003, 13:473-481
58. Ciechanover A: Intracellular protein degradation: from a vague idea thru the lysosome and the ubiquitin-proteasome system and onto human diseases and drug targeting. Cell Death Differ 2005, 12:1178-1190
59. d'Azzo A, Bongiovanni A, Nastasi T: E3 ubiquitin ligases as regulators of membrane protein trafficking and degradation. Traffic 2005, 6:429-441
60. Jin LW, Maezawa I, Vincent I, Bird T: Intracellular accumulation of amyloidogenic fragments of amyloid-β precursor protein in neurons with Niemann-Pick type C defects is associated with endosomal abnormalities. Am J Pathol 2004, 164:975-985
61. Tanida I, Minematsu-lkeguchi N, Ueno T, Kominami E: Lysosomal turnover, but not a cellular level, of endogenous LC3 is a marker for autophagy. Autophagy 2005, 1:84-91
62. Koike M, Shibata M, Waguri S, Yoshimura K, Tanida I, Kominami E, Gotow T, Peters C, von Figura K, Mizushima N, Saftig P, Uchiyama Y: Participation of autophagy in storage of lysosomes in neurons from mouse models of neuronal ceroid-lipofuscinoses (Batten disease). Am J Pathol 2005, 167:1713-1728
63. Stefanis L, Larsen KE, Rideout HJ, Sulzer D, Greene LA: Expression of A53T mutant but not wild-type α-synuclein in PC12 cells induces alterations of the ubiquitin-dependent degradation system, loss of dopamine release, and autophagic cell death. J Neurosci 2001, 21:9549-9560
64. Florez-McClure ML, Linseman DA, Chu CT, Barker PA, Bouchard RJ, Le SS, Laessig TA, Heidenreich KA: The p75 neurotrophin receptor can induce autophagy and death of cerebellar Purkinje neurons. J Neurosci 2004, 24:4498-4509
65. Yue Z, Horton A, Bravin M, DeJager PL, Selimi F, Heintz N: A novel protein complex linking the delta 2 glutamate receptor and autophagy: implications for neurodegeneration in lurcher mice. Neuron 2002, 35:921-933
66. Selimi F, Lohof AM, Heitz S, Lalouette A, Jarvis CI, Bailly Y, Mariani J: Lurcher GRID2-induced death and depolarization can be dissociated in cerebellar Purkinje cells. Neuron 2003, 37:813-819
67. Mizushima N, Ohsumi Y, Yoshimori T: Autophagosome formation in mammalian cells. Cell Struct Funct 2002, 27:421-429
68. Paquet C, Sane AT, Beauchemin M, Bertrand R: Caspase- and mitochondrial dysfunction-dependent mechanisms of lysosomal leakage and cathepsin B activation in DNA damage-induced apoptosis. Leukemia 2005, 19:784-791
69. Hara T, Nakamura K, Matsui M, Yamamoto A, Nakahara Y, Suzuki-Migishima R, Yokoyama M, Mishima K, Saito I, Okano H, Mizushima N: Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 2006, 441:885-889
70. Komatsu M, Waguri S, Chiba T, Murata S, Iwata J, Tanida I, Ueno T, Koike M, Uchiyama Y, Kominami E, Tanaka K: Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 2006, 441:880-884
71. González-Polo RA, Boya P, Pauleau AL, Jalil A, Larochette N, Souquere S, Eskelinen EL, Pierron G, Saftig P, Kroemer G: The apoptosis/autophagy paradox: autophagic vacuolization before apoptotic death. J Cell Sci 2005, 118:3091-3102
72. Boya P, Gonzalez-Polo RA, Casares N, Perfettini JL, Dessen P, Larochette N, Metivier D, Meley D, Souquere S, Yoshimori T, Pierron G, Codogno P, Kroemer G: Inhibition of macroautophagy triggers apoptosis. Mol Cell Biol 2005, 25:1025-1040