Ablation of vacuole protein sorting 18 (Vps18) gene leads to neurodegeneration and impaired neuronal migration by disrupting multiple vesicle transport pathways to lysosomes

Journal of Biological Chemistry

Volumn 287, Issue 39, 2012, Pages 32861-32873

  Peng, Chao ^a   Ye, Jian ^a   Yan, Shunfei ^a   Kong, Shanshan ^a   Shen, Ye ^a   Li, Chenyu ^a   Li, Qinyu ^a   Zheng, Yufang ^a   Deng, Kejing ^a   Xu, Tian ^a,b   Tao, Wufan ^a  

^a FUDAN UNIVERSITY   (China)

^b YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AUTOPHAGY; BIOSYNTHETIC PATHWAY; CENTRAL NERVOUS SYSTEMS; CORE COMPLEX; INTEGRINS; INTRACELLULAR VESICLES; KNOCK OUTS; MECHANISTIC STUDIES; MOUSE BRAIN; NEURAL CELLS; NEURAL DISORDERS; NEURODEGENERATION; NEURONAL MIGRATION; NEURONAL SURVIVAL; PHYSIOLOGICAL FUNCTIONS; PROTEIN SORTING; UP-REGULATION; VESICLE TRANSPORT;

ABLATION; DEFECTS; MAMMALS; MOLECULAR BIOLOGY;

NEURONS;

BETA1 INTEGRIN; CELL PROTEIN; NERVE CELL ADHESION MOLECULE; NESTIN; REELIN; STRESS ACTIVATED PROTEIN KINASE; UNCLASSIFIED DRUG; VPS18 PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOPHAGY; BIOSYNTHESIS; BRAIN DEVELOPMENT; BRAIN NERVE CELL; CELL MIGRATION; CELL SURVIVAL; CELL TRANSPORT; CELL VACUOLE; CONTROLLED STUDY; DISEASE SEVERITY; ENDOCYTOSIS; ENZYME ACTIVATION; GENE; GENE DELETION; GENE SILENCING; LYSOSOME; MOUSE; NERVE DEGENERATION; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; UPREGULATION; VPS18 GENE;

ANIMALS; ANTIGENS, CD29; BIOLOGICAL TRANSPORT, ACTIVE; BRAIN; CADHERINS; CELL MOVEMENT; GENE EXPRESSION REGULATION; LYSOSOMES; MICE; MICE, MUTANT STRAINS; NERVE TISSUE PROTEINS; NEURODEGENERATIVE DISEASES; NEURONS; VESICULAR TRANSPORT PROTEINS;

MAMMALIA; MUS;

EID: 84866551638     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M112.384305     Document Type: Article

References (49)

1. Cheung, Z. H., and Ip, N. Y. (2011) Autophagy deregulation in neurodegenerative diseases: recent advances and future perspectives. J. Neurochem. 118, 317-325
2. Zhang, M. (2008) Endocytic mechanisms and drug discovery in neurodegenerative diseases. Front. Biosci. 13, 6086-6105
3. Nixon, R. A. (2005) Endosome function and dysfunction in Alzheimer disease and other neurodegenerative diseases. Neurobiol. Aging 26, 373-382
4. Hara, T., Nakamura, K., Matsui, M., Yamamoto, A., Nakahara, Y., Suzuki-Migishima, R., Yokoyama, M., Mishima, K., Saito, I., Okano, H., and Mizushima, N. (2006) Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature 441, 885-889
5. Komatsu, M., Waguri, S., Chiba, T., Murata, S., Iwata, J., Tanida, I., Ueno, T., Koike, M., Uchiyama, Y., Kominami, E., and Tanaka, K. (2006) Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature 441, 880-884
6. Jalanko, A., and Braulke, T. (2009) Neuronal ceroid lipofuscinoses. Biochim. Biophys. Acta 1793, 697-709
7. Felbor, U., Kessler, B., Mothes, W., Goebel, H. H., Ploegh, H. L., Bronson, R. T., and Olsen, B. R. (2002) Neuronal loss and brain atrophy in mice lacking cathepsins B and L. Proc. Natl. Acad. Sci. U.S.A. 99, 7883-7888 (Pubitemid 34650974)
8. Hatten, M. E. (1999) Central nervous system neuronal migration. Annu. Rev. Neurosci. 22, 511-539
9. Trommsdorff, M., Gotthardt, M., Hiesberger, T., Shelton, J., Stockinger, W., Nimpf, J., Hammer, R. E., Richardson, J. A., and Herz, J. (1999) Reeler/Disabled-like disruption of neuronal migration in knockout mice lacking the VLDL receptor and ApoE receptor 2. Cell 97, 689-701 (Pubitemid 29278044)
10. Cooper, J. A. (2008) A mechanism for inside-out lamination in the neocortex. Trends Neurosci. 31, 113-119
11. Schmid, R. S., Jo, R., Shelton, S., Kreidberg, J. A., and Anton, E. S. (2005) Reelin, integrin and DAB1 interactions during embryonic cerebral cortical development. Cereb. Cortex 15, 1632-1636 (Pubitemid 41344512)
12. Belvindrah, R., Graus-Porta, D., Goebbels, S., Nave, K. A., and Müller, U. (2007) β1 integrins in radial glia but not in migrating neurons are essential for the formation of cell layers in the cerebral cortex. J. Neurosci. 27, 13854-13865 (Pubitemid 350278262)
13. Stanco, A., Szekeres, C., Patel, N., Rao, S., Campbell, K., Kreidberg, J. A., Polleux, F., and Anton, E. S. (2009) Netrin-1-α3β1 integrin interactions regulate the migration of interneurons through the cortical marginal zone. Proc. Natl. Acad. Sci. U.S.A. 106, 7595-7600
14. Kawauchi, T., Sekine, K., Shikanai, M., Chihama, K., Tomita, K., Kubo, K., Nakajima, K., Nabeshima, Y., and Hoshino, M. (2010) Rab GTPase-dependent endocytic pathways regulate neuronal migration and maturation through N-cadherin trafficking. Neuron 67, 588-602
15. Rieder, S. E., and Emr, S. D. (1997) A novel RING finger protein complex essential for a late step in protein transport to the yeast vacuole. Mol. Biol. Cell 8, 2307-2327 (Pubitemid 27469390)
16. Nickerson, D. P., Brett, C. L., and Merz, A. J. (2009) Vps-C complexes: gatekeepers of endolysosomal traffic. Curr. Opin. Cell Biol. 21, 543-551
17. Lindmo, K., Simonsen, A., Brech, A., Finley, K., Rusten, T. E., and Stenmark, H. (2006) A dual function for Deep orange in programmed autophagy in the Drosophila melanogaster fat body. Exp. Cell Res. 312, 2018-2027 (Pubitemid 43850927)
18. Sevrioukov, E. A., He, J. P., Moghrabi, N., Sunio, A., and Krämer, H. (1999) A role for the deep orange and carnation eye color genes in lysosomal delivery in Drosophila. Mol. Cell 4, 479-486 (Pubitemid 29531128)
19. Chi, C., Zhu, H., Han, M., Zhuang, Y., Wu, X., and Xu, T. (2010) Disruption of lysosome function promotes tumor growth and metastasis in Drosophila. J. Biol. Chem. 285, 21817-21823
20. Maldonado, E., Hernandez, F., Lozano, C., Castro, M. E., and Navarro, R. E. (2006) The zebrafish mutant vps18 as a model for vesicle-traffic related hypopigmentation diseases. Pigment Cell Res. 19, 315-326 (Pubitemid 44015594)
21. Sadler, K. C., Amsterdam, A., Soroka, C., Boyer, J., and Hopkins, N. (2005) A genetic screen in zebrafish identifies the mutants vps18, nf2, and foie gras as models of liver disease. Development 132, 3561-3572 (Pubitemid 41246129)
22. Liang, C., Lee, J. S., Inn, K. S., Gack, M. U., Li, Q., Roberts, E. A., Vergne, I., Deretic, V., Feng, P., Akazawa, C., and Jung, J. U. (2008) Beclin1-binding UVRAG targets the class C Vps complex to coordinate autophagosome maturation and endocytic trafficking. Nat. Cell Biol. 10, 776-787 (Pubitemid 351927707)
23. Richardson, S. C., Winistorfer, S. C., Poupon, V., Luzio, J. P., and Piper, R. C. (2004) Mammalian late vacuole protein sorting orthologues participate in early endosomal fusion and interact with the cytoskeleton. Mol. Biol. Cell 15, 1197-1210 (Pubitemid 38316227)
24. Dong, Y., Du, X., Ye, J., Han, M., Xu, T., Zhuang, Y., and Tao, W. (2009) A cell-intrinsic role for Mst1 in regulating thymocyte egress. J. Immunol. 183, 3865-3872
25. Harlow, E., and Lane, D. (1999) Using Antibodies: A Laboratory Manual, Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY
26. Saito, T. (2006) In vivo electroporation in the embryonic mouse central nervous system. Nat. Protoc. 1, 1552-1558
27. 2-terminal kinase signaling mediates collagen I-induced cell scattering and up-regulation of N-cadherin expression in mouse mammary epithelial cells. Mol. Biol. Cell 17, 2963-2975
28. International Mouse Knockout Consortium, Collins, F. S., Rossant, J., and Wurst, W. (2007) A mouse for all reasons. Cell 128, 9-13
29. Barski, J. J., Dethleffsen, K., and Meyer, M. (2000) Cre recombinase expression in cerebellar Purkinje cells. Genesis 28, 93-98
30. Yuasa, S., Kawamura, K., Ono, K., Yamakuni, T., and Takahashi, Y. (1991) Development and migration of Purkinje cells in the mouse cerebellar primordium. Anat. Embryol. 184, 195-212
31. Zhou, X., Wang, L., Hasegawa, H., Amin, P., Han, B. X., Kaneko, S., He, Y., and Wang, F. (2010) Deletion of PIK3C3/Vps34 in sensory neurons causes rapid neurodegeneration by disrupting the endosomal but not the autophagic pathway. Proc. Natl. Acad. Sci. U.S.A. 107, 9424-9429
32. Kunwar, A. J., Rickmann, M., Backofen, B., Browski, S. M., Rosenbusch, J., Schöning, S., Fleischmann, T., Krieglstein, K., and Fischer von Mollard, G. (2011) Lack of the endosomal SNAREs vti1a and vti1b led to significant impairments in neuronal development. Proc. Natl. Acad. Sci. U.S.A. 108, 2575-2580
33. Kabeya, Y., Mizushima, N., Ueno, T., Yamamoto, A., Kirisako, T., Noda, T., Kominami, E., Ohsumi, Y., and Yoshimori, T. (2000) LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 19, 5720-5728
34. Mizushima, N., and Hara, T. (2006) Intracellular quality control by autophagy: how does autophagy prevent neurodegeneration? Autophagy 2, 302-304 (Pubitemid 44342375)
35. Komatsu, M., Waguri, S., Koike, M., Sou, Y. S., Ueno, T., Hara, T., Mizushima, N., Iwata, J., Ezaki, J., Murata, S., Hamazaki, J., Nishito, Y., Iemura, S., Natsume, T., Yanagawa, T., Uwayama, J., Warabi, E., Yoshida, H., Ishii, T., Kobayashi, A., Yamamoto, M., Yue, Z., Uchiyama, Y., Kominami, E., and Tanaka, K. (2007) Homeostatic levels of p62 control cytoplasmic inclusion body formation in autophagy-deficient mice. Cell 131, 1149-1163 (Pubitemid 350235021)
36. Duit, S., Mayer, H., Blake, S. M., Schneider, W. J., and Nimpf, J. (2010) Differential functions of ApoER2 and very low density lipoprotein receptor in Reelin signaling depend on differential sorting of the receptors. J. Biol. Chem. 285, 4896-4908
37. Hashimoto-Torii, K., Torii, M., Sarkisian, M. R., Bartley, C. M., Shen, J., Radtke, F., Gridley, T., Sestan, N., and Rakic, P. (2008) Interaction between Reelin and Notch signaling regulates neuronal migration in the cerebral cortex. Neuron 60, 273-284
38. Graus-Porta, D., Blaess, S., Senften, M., Littlewood-Evans, A., Damsky, C., Huang, Z., Orban, P., Klein, R., Schittny, J. C., and Müller, U. (2001) β1 class integrins regulate the development of laminae and folia in the cerebral and cerebellar cortex. Neuron 31, 367-379 (Pubitemid 32778557)
39. Schmid, R. S., Shelton, S., Stanco, A., Yokota, Y., Kreidberg, J. A., and Anton, E. S. (2004) α3β1 integrin modulates neuronal migration and placement during early stages of cerebral cortical development. Development 131, 6023-6031 (Pubitemid 40123917)
40. Lobert, V. H., Brech, A., Pedersen, N. M., Wesche, J., Oppelt, A., Malerød, L., and Stenmark, H. (2010) Ubiquitination of α5β1 integrin controls fibroblast migration through lysosomal degradation of fibronectin-integrin complexes. Dev. Cell 19, 148-159
41. Jung, A. R., Kim, T. W., Rhyu, I. J., Kim, H., Lee, Y. D., Vinsant, S., Oppenheim, R. W., and Sun, W. (2008) Misplacement of Purkinje cells during postnatal development in Bax knock-out mice: a novel role for programmed cell death in the nervous system? J. Neurosci. 28, 2941-2948 (Pubitemid 351398868)
42. Chintala, S., Novak, E. K., Spernyak, J. A., Mazurchuk, R., Torres, G., Patel, S., Busch, K., Meeder, B. A., Horowitz, J. M., Vaughan, M. M., and Swank, R. T. (2009) The Vps33a gene regulates behavior and cerebellar Purkinje cell number. Brain Res. 1266, 18-28
43. Ostrowicz, C. W., Bröcker, C., Ahnert, F., Nordmann, M., Lachmann, J., Peplowska, K., Perz, A., Auffarth, K., Engelbrecht-Vandré, S., and Ungermann, C. (2010) Defined subunit arrangement and Rab interactions are required for functionality of the HOPS tethering complex. Traffic 11, 1334-1346
44. Yu, W. H., Cuervo, A. M., Kumar, A., Peterhoff, C. M., Schmidt, S. D., Lee, J. H., Mohan, P. S., Mercken, M., Farmery, M. R., Tjernberg, L. O., Jiang, Y., Duff, K., Uchiyama, Y., Näslund, J., Mathews, P. M., Cataldo, A. M., and Nixon, R. A. (2005) Macroautophagy-a novel β-amyloid peptide-generating pathway activated in Alzheimer disease. J. Cell Biol. 171, 87-98 (Pubitemid 41434604)
45. Boland, B., Kumar, A., Lee, S., Platt, F. M., Wegiel, J., Yu, W. H., and Nixon, R. A. (2008) Autophagy induction and autophagosome clearance in neurons: relationship to autophagic pathology in Alzheimer disease. J. Neurosci. 28, 6926-6937
46. Hook, V., Schechter, I., Demuth, H. U., and Hook, G. (2008) Alternative pathways for production of β-amyloid peptides of Alzheimer disease. Biol. Chem. 389, 993-1006
47. Anton, E. S., Kreidberg, J. A., and Rakic, P. (1999) Distinct functions of α3 and αv integrin receptors in neuronal migration and laminar organization of the cerebral cortex. Neuron 22, 277-289 (Pubitemid 29109662)
48. Yuasa, S., Kitoh, J., Oda, S., and Kawamura, K. (1993) Obstructed migration of Purkinje cells in the developing cerebellum of the Reeler mutant mouse. Anat. Embryol. 188, 317-329 (Pubitemid 23305153)
49. Weiss, K. H., Johanssen, C., Tielsch, A., Herz, J., Deller, T., Frotscher, M., and Förster, E. (2003) Malformation of the radial glial scaffold in the dentate gyrus of Reeler mice, scrambler mice, and ApoER2/VLDLR-deficient mice. J. Comp. Neurol. 460, 56-65 (Pubitemid 36438277)