Macroautophagy - A novel β-amyloid peptide-generating pathway activated in Alzheimer's disease

Journal of Cell Biology

Volumn 171, Issue 1, 2005, Pages 87-98

  Haung Yu, W ^a,b   Cuervo, Ana Maria ^c   Kumar, Asok ^a   Peterhoff, Corrinne M ^a   Schmidt, Stephen D ^a   Lee, Ju Hyun ^a,b   Mohan, Panaiyur S ^a,b   Mercken, Marc ^d   Farmery, Mark R ^e   Tjernberg, Lars O ^e   Jiang, Ying ^a,b   Duff, Karen ^a,b   Uchiyama, Yasuo ^f   Näslund, Jan ^e   Mathews, Paul M ^a,b   Cataldo, Anne M ^g   Nixon, Ralph A ^a,b  

^a NATHAN S KLINE INSTITUTE FOR PSYCHIATRIC RESEARCH   (United States)

^b NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^d JANSSEN RESEARCH FOUNDATION   (Belgium)

^e KAROLINSKA INSTITUTE   (Sweden)

^f OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^g MCLEAN HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; GAMMA SECRETASE; NICASTRIN; PRESENILIN 1;

ADULT; AGED; ALZHEIMER DISEASE; AMYLOIDOSIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY LABELING; ARTICLE; AUTOPHAGY; CELL MATURATION; CELL PROLIFERATION; CELL SURVIVAL; CELL VACUOLE; CONTROLLED STUDY; DENDRITE; DYSTROPHY; ENZYME ACTIVITY; EXPERIMENTAL MODEL; FEMALE; HUMAN; HUMAN TISSUE; MALE; MOUSE; NERVE CELL; NONHUMAN; PHAGOSOME; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ADULT; AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN; AMYLOID BETA-PROTEIN PRECURSOR; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ASPARTIC ENDOPEPTIDASES; AUTOPHAGY; BRAIN; ENDOPEPTIDASES; FEMALE; HUMANS; MALE; MEMBRANE PROTEINS; MICE; MICROSCOPY, IMMUNOELECTRON; MIDDLE AGED; MODELS, MOLECULAR; MUTATION; PRESENILIN-1; SIGNAL TRANSDUCTION; VACUOLES;

MAMMALIA;

EID: 26444587508     PISSN: 00219525     EISSN: 00219525     Source Type: Journal    
DOI: 10.1083/jcb.200505082     Document Type: Article

References (71)

1. Asanuma, K., I. Tanida, I. Shirato, T. Ueno, H. Takahara, T. Nishitani, E. Kominami, and Y. Tomino. 2003. MAP-LC3, a promising autophagosomal marker, is processed during the differentiation and recovery of podocytes from PAN nephrosis. FASEB J. 17:1165-1167.
2. Askanas, V., W.K. Engel, C.C. Yang, R.B. Alvarez, V.M. Lee, and T. Wisniewski. 1998. Light and electron microscopic immunolocalization of presenilin 1 in abnormal muscle fibers of patients with sporadic inclusion-body myositis and autosomal-recessive inclusion-body myopathy. Am. J. Pathol. 152:889-895.
3. Bendiske, J., and B.A. Bahr. 2003. Lysosomal activation is a compensatory response against protein accumulation and associated synaptopathogenesis-an approach for slowing Alzheimer disease? J. Neuropathol. Exp. Neurol. 62:451-463.
4. Biederbick, A., H.F. Kern, and H.P. Elsasser. 1995. Monodansylcadaverine (MDC) is a specific in vivo marker for autophagic vacuoles. Eur. J. Cell Biol. 66:3-14.
5. Billings, L.M., S. Oddo, K.N. Green, J.L. McGaugh, and F.M. Laferla. 2005. Intraneuronal A causes the onset of early Alzheimer's disease-related cognitive deficits in transgenic mice. Neuron. 45:675-688.
6. Boya, P., R.A. Gonzalez-Polo, N. Casares, J.L. Perfettini, P. Dessen, N. Larochette, D. Metivier, D. Meley, S. Souquere, T. Yoshimori, et al. 2005. Inhibition of macroautophagy triggers apoptosis. Mol. Cell. Biol. 25:1025-1040.
7. Braak, H., and E. Braak. 1991. Neuropathological staging of Alzheimer-related changes. Acta Neuropathol. (Berl.). 82:239-259.
8. Brunk, U.T., and A. Terman. 2002. The mitochondrial-lysosomal axis theory of aging: accumulation of damaged mitochondria as a result of imperfect autophagocytosis. Eur. J. Biochem. 269:1996-2002.
9. Bursch, W. 2001. The autophagosomal-lysosomal compartment in programmed cell death. Cell Death Differ. 8:569-581.
10. Cataldo, A.M., J.L. Barnett, D.M. Mann, and R.A. Nixon. 1996. Colocalization of lysosomal hydrolase and beta-amyloid in diffuse plaques of the cerebellum and striatum in Alzheimer's disease and Down's syndrome. J. Neuropathol. Exp. Neurol. 55:704-715.
11. Cataldo, A.M., S. Petanceska, N.B. Terio, C.M. Peterhoff, J.C. Troncoso, R. Durham, M. Mercken, P.D. Mehta, J.D. Buxbaum, V. Haroutunian, and R.A. Nixon. 2004a. Aβ localization to abnormal endosomes coincides with early increases in soluble Aβ in Alzheimer's disease brain. Neurobiol. Aging. 25:1263-1272.
12. Cataldo, A.M., C.M. Peterhoff, S.D. Schmidt, N.B. Terio, K. Duff, M. Beard, P.M. Mathews, and R.A. Nixon. 2004b. Presenilin mutations in familial Alzheimer disease and transgenic mouse models accelerate neuronal lysosomal pathology. J. Neuropathol. Exp. Neurol. 63:821-830.
13. Clarke, P.G. 1990. Developmental cell death: morphological diversity and multiple mechanisms. Anat. Embryol. (Berl.). 181:195-213.
14. Cuervo, A.M., and J.F. Dice. 2000. Age-related decline in chaperone-mediated autophagy. J. Biol. Chem. 275:31505-31513.
15. Cuervo, A.M., L. Stefanis, R. Fredenburg, P.T. Lansbury, and D. Sulzer. 2004. Impaired degradation of mutant α-synuclein by chaperone-mediated autophagy. Science. 305:1292-1295.
16. Culvenor, J.G., F. Maher, G. Evin, F. Malchiodi-Albedi, R. Cappai, J.R. Underwood, J.B. Davis, E.H. Karran, G.W. Roberts, K. Beyreuther, and C.L. Masters. 1997. Alzheimer's disease-associated presenilin 1 in neuronal cells: evidence for localization to the endoplasmic reticulum-Golgi intermediate compartment. J. Neurosci. Res. 49:719-731.
17. Cupers, P., M. Bentahir, K. Craessaerts, I. Orlans, H. Vanderstichele, P. Saftig, B. De Strooper, and W. Annaert. 2001. The discrepancy between presenilin subcellular localization and γ-secretase processing of amyloid precursor protein. J. Cell Biol. 154:731-740.
18. Duff, K., C. Eckman, C. Zehr, X. Yu, C.M. Prada, J. Perez-tur, M. Hutton, L. Buee, Y. Harigaya, D. Yager, et al. 1996. Increased amyloid-β42(43) in brains of mice expressing mutant presenilin 1. Nature. 383:710-713.
19. Dunn, W.A., Jr. 1990a. Studies on the mechanisms of autophagy: formation of the autophagic vacuole. J. Cell Biol. 110:1923-1933.
20. Dunn, W.A., Jr. 1990b. Studies on the mechanisms of autophagy: maturation of the autophagic vacuole. J. Cell Biol. 110:1935-1945.
21. Edbauer, D., E. Winkler, J.T. Regula, B. Pesold, H. Steiner, and C. Haass. 2003. Reconstitution of gamma-secretase activity. Nat. Cell Biol. 5:486-488.
22. Farmery, M.R., L.O. Tjernberg, S.E. Pursglove, A. Bergman, B. Winblad, and J. Naslund. 2003. Partial purification and characterization of gamma-secretase from post-mortem human brain. J. Biol. Chem. 278:24277-24284.
23. Fevrier, B., D. Vilette, H. Laude, and G. Raposo. 2005. Exosomes: a bubble ride for prions? Traffic. 6:10-17.
24. Fuertes, G., J.J. Martin De Llano, A. Villarroya, A.J. Rivett, and E. Knecht. 2003. Changes in the proteolytic activities of proteasomes and lysosomes in human fibroblasts produced by serum withdrawal, amino-acid deprivation and confluent conditions. Biochem. J. 375:75-86.
25. Gordon, P.B., and P.O. Seglen. 1988. Prelysosomal convergence of autophagic and endocytic pathways. Biochem. Biophys. Res. Commun. 151:40-47.
26. Gozuacik, D., and A. Kimchi. 2004. Autophagy as a cell death and tumor suppressor mechanism. Oncogene. 23:2891-2906.
27. Grbovic, O.M., P.M. Mathews, Y. Jiang, S.D. Schmidt, R. Dinakar, N.B. Summers-Terio, B.P. Ceresa, R.A. Nixon, and A.M. Cataldo. 2003. Rab5-stimulated up-regulation of the endocytic pathway increases intracellular beta-cleaved amyloid precursor protein carboxyl-terminal fragment levels and Aβ production. J. Biol. Chem. 278:31261-31268.
28. Gyure, K.A., R. Durham, W.F. Stewart, J.E. Smialek, and J.C. Troncoso. 2001. Intraneuronal abeta-amyloid precedes development of amyloid plaques in Down syndrome. Arch. Pathol. Lab. Med. 125:489-492.
29. Holcomb, L., M.N. Gordon, E. McGowan, X. Yu, S. Benkovic, P. Jantzen, K. Wright, I. Saad, R. Mueller, D. Morgan, et al. 1998. Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes. Nat. Med. 4:97-100.
30. Hollenbeck, P.J. 1993. Products of endocytosis and autophagy are retrieved from axons by regulated retrograde organelle transport. J. Cell Biol. 121:305-315.
31. Jackson, W.T., T.H. Giddings Jr., M.P. Taylor, S. Mulinyawe, M. Rabinovitch, R.R. Kopito, and K. Kirkegaard. 2005. Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol. 10.1371/journal.pbio. 0030156.
32. Kabeya, Y., N. Mizushima, T. Ueno, A. Yamamoto, T. Kirisako, T. Noda, E. Kominami, Y. Ohsumi, and T. Yoshimori. 2000. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19:5720-5728.
33. Kabeya, Y., N. Mizushima, A. Yamamoto, S. Oshitani-Okamoto, Y. Ohsumi, and T. Yoshimori. 2004. LC3, GABARAP and GATE16 localize to autophagosomal membrane depending on form-II formation. J. Cell Sci. 117:2805-2812.
34. Kadowaki, M., and T. Kanazawa. 2003. Amino acids as regulators of proteolysis. J. Nutr. 133:2052S-2056S.
35. Kanazawa, T., I. Taneike, R. Akaishi, F. Yoshizawa, N. Furuya, S. Fujimura, and M. Kadowaki. 2003. Amino acids and insulin control autophagic proteolysis through different signaling pathways in relation to mTOR in isolated rat hepatocytes. J Biol Chem. 279:8452-8459.
36. Kanzawa, T., I.M. Germano, T. Komata, H. Ito, Y. Kondo, and S. Kondo. 2004. Role of autophagy in temozolomide-induced cytotoxicity for malignant glioma cells. Cell Death Differ. 11:448-457.
37. Lai, M.T., E. Chen, M.C. Crouthamel, J. DiMuzio-Mower, M. Xu, Q. Huang, E. Price, R.B. Register, X.P. Shi, D.B. Donoviel, et al. 2003. Presenilin-1 and presenilin-2 exhibit distinct yet overlapping γ-secretase activities. J. Biol. Chem. 278:22475-22481.
38. Leuba, G., G. Wernli, A. Vernay, R. Kraftsik, M.H. Mohajeri, and K.D. Saini. 2005. Neuronal and nonneuronal quantitative BACE immunocytochemical expression in the entorhinohippocampal and frontal regions in Alzheimer's Disease. Dement. Geriatr. Cogn. Disord. 19:171-183.
39. Luzio, J.P., P.R. Pryor, S.R. Gray, M.J. Gratian, R.C. Piper, and N.A. Bright. 2005. Membrane traffic to and from lysosomes. Biochem. Soc. Symp. 2005:77-86.
40. Marzella, L., J. Ahlberg, and H. Glaumann. 1982. Isolation of autophagic vacuoles from rat liver: morphological and biochemical characterization. J. Cell Biol. 93:144-154.
41. Masliah, E., M. Mallory, T. Deerinck, R. DeTeresa, S. Lamont, A. Miller, R.D. Terry, B. Carragher, and M. Ellisman. 1993. Re-evaluation of the structural organization of the neuritic plaques in Alzheimer's disease. J. Neuropathol. Exp. Neurol. 52:619-632.
42. Mathews, P.M., Y. Jiang, S.D. Schmidt, O.M. Grbovic, M. Mercken, and R.A. Nixon. 2002. Calpain activity regulates the cell surface distribution of amyloid precursor protein. J. Biol. Chem. 277:36415-36424.
43. Matsuoka, Y., M. Picciano, J. La Francois, and K. Duff. 2001. Fibrillar β-amyloid evokes oxidative damage in a transgenic mouse model of Alzheimer's disease. Neuroscience. 104:609-613.
44. Meijer, A.J., and P. Codogno. 2004. Regulation and role of autophagy in mammalian cells. Int. J. Biochem. Cell Biol. 36:2445-2462.
45. Melendez, A., Z. Talloczy, M. Seaman, E.L. Eskelinen, D.H. Hall, and B. Levine. 2003. Autophagy genes are essential for dauer development and life-span extension in C. elegans. Science. 301:1387-1391.
46. Mirra, S.S., A. Heyman, D. McKeel, S.M. Sumi, B.J. Crain, L.M. Brownlee, F.S. Vogel, J.P. Hughes, G. van Belle, and L. Berg. 1991. The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease. Neurology. 41:479-486.
47. Mirra, S.S., M.N. Hart, and R.D. Terry. 1993. Making the diagnosis of Alzheimer's disease. A primer for practicing pathologists. Arch. Pathol. Lab. Med. 117:132-144.
48. Mizushima, N., A. Yamamoto, M. Matsui, T. Yoshimori, and Y. Ohsumi. 2004. In vivo analysis of autophagy in response to nutrient starvation using transgenic mice expressing a fluorescent autophagosome marker. Mol. Biol. Cell. 15:1101-1111.
49. Mortimore, G.E., and C.M. Schworer. 1977. Induction of autophagy by aminoacid deprivation in perfused rat liver. Nature. 270:174-176.
50. Munafo, D.B., and M.I. Colombo. 2002. Induction of autophagy causes dramatic changes in the subcellular distribution of GFP-Rab24. Traffic. 3:472-482.
51. Newell, K.L., B.T. Hyman, J.H. Growdon, and E.T. Hedley-Whyte. 1999. Application of the National Institute on Aging (NIA)-Reagan Institute criteria for the neuropathological diagnosis of Alzheimer disease. J. Neuropathol. Exp. Neurol. 58:1147-1155.
52. Nixon, R.A., A.M. Cataldo, and P.M. Mathews. 2000. The endosomal-lysosomal system of neurons in Alzheimer's disease pathogenesis: a review. Neurochem. Res. 25:1161-1172.
53. Nixon, R.A., P.M. Mathews, and A.M. Cataldo. 2001. The neuronal endosomallysosomal system in Alzheimer's disease. J. Alzheimers Dis. 3:97-107.
54. Nixon, R.A., J. Wegiel, A. Kumar, W.H. Yu, C. Peterhoff, A. Cataldo, and A.M. Cuervo. 2005. Extensive involvement of autophagy in Alzheimer disease: an immunoelectron microscopy study. J. Neuropathol. Exp. Neurol. 64:113-122.
55. Noda, T., and Y. Ohsumi. 1998. Tor, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J. Biol. Chem. 273:3963-3966.
56. Overly, C.C., and P.J. Hollenbeck. 1996. Dynamic organization of endocytic pathways in axons of cultured sympathetic neurons. J. Neurosci. 16: 6056-6064.
57. Pasternak, S.H., R.D. Bagshaw, M. Guiral, S. Zhang, C.A. Ackerley, B.J. Pak, J.W. Callahan, and D.J. Mahuran. 2003. Presenilin-1, nicastrin, amyloid precursor protein, and γ-secretase activity are co-localized in the lysosomal membrane. J. Biol. Chem. 278:26687-26694.
58. Petanceska, S.S., M. Seeger, F. Checler, and S. Gandy. 2000. Mutant presenilin 1 increases the levels of Alzheimer amyloid beta-peptide Aβ42 in late compartments of the constitutive secretory pathway. J. Neurochem. 74:1878-1884.
59. Petiot, A., E. Ogier-Denis, E.F. Blommaart, A.J. Meijer, and P. Codogno. 2000. Distinct classes of phosphatidylinositol 3′-kinases are involved in signaling pathways that control macroautophagy in HT-29 cells. J. Biol. Chem. 275:992-998.
60. Ravikumar, B., C. Vacher, Z. Berger, J.E. Davies, S. Luo, L.G. Oroz, F. Scaravilli, D.F. Easton, R. Duden, C.J. O'Kane, and D.C. Rubinsztein. 2004. Inhibition of mTOR induces autophagy and reduces toxicity of polyglutamine expansions in fly and mouse models of Huntington disease. Nat. Genet. 36:585-595.
61. Rubinsztein, D.C., M. DiFiglia, N. Heinta, R.A. Nixon, Z.-H. Qin, B. Ravikumar, L. Stefanis, and A. Tolkovsky. 2005. Autophagy and its possible roles in nervous system diseases, damage and repair. Autophagy. 1:11-22.
62. Seglen, P.O., and P.B. Gordon. 1984. Amino acid control of autophagic sequestration and protein degradation in isolated rat hepatocytes. J. Cell Biol. 99:435-444.
63. Seglen, P.O., P.B. Gordon, H. Tolleshaug, and H. Hoyvik. 1986. Use of [3H]raffinose as a specific probe of autophagic sequestration. Exp. Cell Res. 162:273-277.
64. Seglen, P.O., T.O. Berg, H. Blankson, M. Fengsrud, I. Holen, and P.E. Stromhaug. 1996. Structural aspects of autophagy. Adv. Exp. Med. Biol. 389:103-111.
65. Shigemitsu, K., Y. Tsujishita, K. Hara, M. Nanahoshi, J. Avruch, and K. Yonezawa. 1999. Regulation of translational effectors by amino acid and mammalian target of rapamycin signaling pathways. Possible involvement of autophagy in cultured hepatoma cells. J. Biol. Chem. 274:1058-1065.
66. Smith, D.H., K. Uryu, K.E. Saatman, J.Q. Trojanowski, and T.K. McIntosh. 2003. Protein accumulation in traumatic brain injury. Neuromolecular Med. 4:59-72.
67. Suzuki, K., and R.D. Terry. 1967. Fine structural localization of acid phosphatase in senile plaques in Alzheimer's presenile dementia. Acta Neuropathol. (Berl.). 8:276-284.
68. Takahashi, R.H., T.A. Milner, F. Li, E.E. Nam, M.A. Edgar, H. Yamaguchi, M.F. Beal, H. Xu, P. Greengard, and G.K. Gouras. 2002. Intraneuronal Alzheimer Aβ42 accumulates in multivesicular bodies and is associated with synaptic pathology. Am. J. Pathol. 161:1869-1879.
69. Vassar, R., and M. Citron. 2000. Aβ-generating enzymes: Recent advances in β-and γ-secretase research. Neuron. 27:419-422.
70. Wegiel, J., K.C. Wang, M. Tarnawski, and B. Lach. 2000. Microglia cells are the driving force in fibrillar plaque formation, whereas astrocytes are a leading factor in plague degradation. Acta Neuropathol. (Berl.). 100:356-364.
71. Yu, W.H., A. Kumar, C. Peterhoff, L. Shapiro Kulnane, Y. Uchiyama, B.T. Lamb, A.M. Cuervo, and R.A. Nixon. 2004. Autophagic vacuoles are enriched in amyloid precursor protein-secretase activities: implications for β-amyloid peptide over-production and localization in Alzheimer's disease. Int. J. Biochem. Cell Biol. 36:2531-2540.