Neuronal expression of Fig4 is both necessary and sufficient to prevent spongiform neurodegeneration

Human Molecular Genetics

Volumn 21, Issue 16, 2012, Pages 3525-3534

  Ferguson, C J ^a   Lenk, G M ^a   Jones, J M ^a   Grant, A E ^a   Winters, J J ^a   Dowling, J J ^a   Giger, R J ^a   Meisler, Miriam H ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; FIG4 PROTEIN; NEURON SPECIFIC ENOLASE; PHOSPHATASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; ASTROCYTE; AUTOPHAGY; BRAIN CORTEX; BRAIN NERVE CELL; BRAIN SPONGIOSIS; BRAIN STEM; CELL SURVIVAL; CELL VACUOLE; CEREBELLUM; CONTROLLED STUDY; GENE EXPRESSION; GENE INACTIVATION; GENE TARGETING; GENETIC ANALYSIS; GLIOSIS; HIPPOCAMPUS; HISTOPATHOLOGY; IMMUNOHISTOCHEMISTRY; LETHALITY; MOUSE; NERVE DEGENERATION; NONHUMAN; NULL ALLELE; PRIORITY JOURNAL; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SURVIVAL; TRANSGENE; TRANSGENIC MOUSE;

ANIMALS; ASTROCYTES; BRAIN; CHARCOT-MARIE-TOOTH DISEASE; FLAVOPROTEINS; GENE EXPRESSION; MICE; MICE, TRANSGENIC; MICROGLIA; NEURODEGENERATIVE DISEASES; NEURONS; SCHWANN CELLS;

EID: 84865089799     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds179     Document Type: Article

References (39)

1. Polymenidou, M. and Cleveland, D.W. (2011) The seeds of neurodegeneration: prion-like spreading in ALS. Cell, 147, 498-508.
2. He, L., Lu, X.Y., Jolly, A.F., Eldridge, A.G., Watson, S.J., Jackson, P.K., Barsh, G.S. and Gunn, T.M. (2003) Spongiform degeneration in mahoganoid mutant mice. Science, 299, 710-712.
3. Overton, J.D. and Leibel, R.L. (2011) Mahoganoid and mahogany mutations rectify the obesity of the yellow mouse by effects on endosomal traffic of MC4R protein. J. Biol. Chem., 286, 18914-18929.
4. He, L., Gunn, T.M., Bouley, D.M., Lu, X.Y., Watson, S.J., Schlossman, S.F., Duke-Cohan, J.S. and Barsh, G.S. (2001) A biochemical function for attractin in agouti-induced pigmentation and obesity. Nat Genet., 27, 40-47.
5. Jiao, J., Sun, K., Walker, W.P., Bagher, P., Cota, C.D. and Gunn, T.M. (2009) Abnormal regulation of TSG101 in mice with spongiform neurodegeneration. Biochim. Biophys. Acta, 1792, 1027-1035.
6. Chow, C.Y., Zhang, Y., Dowling, J.J., Jin, N., Adamska, M., Shiga, K., Szigeti, K., Shy, M.E., Li, J., Zhang, X. et al. (2007) Mutation of FIG4 causes neurodegeneration in the pale tremor mouse and patients with CMT4J. Nature, 448, 68-72.
7. Zhang, Y., Zolov, S.N., Chow, C.Y., Slutsky, S.G., Richardson, S.C., Piper, R.C., Yang, B., Nau, J.J., Westrick, R.J., Morrison, S.J. et al. (2007) Loss of Vac14, a regulator of the signaling lipid phosphatidylinositol 3,5-bisphosphate, results in neurodegeneration in mice. Proc. Natl Acad. Sci. USA, 104, 17518-17523.
8. Jin, N., Chow, C.Y., Liu, L., Zolov, S.N., Bronson, R., Davisson, M., Petersen, J.L., Zhang, Y., Park, S., Duex, J.E. et al. (2008) VAC14 nucleates a protein complex essential for the acute interconversion of PI3P and PI(3,5)P(2) in yeast and mouse. EMBO J., 27, 3421-3434.
9. Rusten, T.E., Vaccari, T., Lindmo, K., Rodahl, L.M., Nezis, I.P., Sem-Jacobsen, C., Wendler, F., Vincent, J.P., Brech, A., Bilder, D. et al. (2007) ESCRTs and Fab1 regulate distinct steps of autophagy. Curr. Biol., 17, 1817-1825.
10. Yamamoto, A., DeWald, D.B., Boronenkov, I.V., Anderson, R.A., Emr, S.D. and Koshland, D. (1995) Novel PI(4)P 5-kinase homologue, Fab1p, essential for normal vacuole function and morphology in yeast. Mol. Biol. Cell., 6, 525-539.
11. Bonangelino, C.J., Catlett, N.L. and Weisman, L.S. (1997) Vac7p, a novel vacuolar protein, is required for normal vacuole inheritance and morphology. Mol. Cell. Biol., 17, 6847-6858.
12. Gary, J.D., Wurmser, A.E., Bonangelino, C.J., Weisman, L.S. and Emr, S.D. (1998) Fab1p is essential for PtdIns(3)P 5-kinase activity and the maintenance of vacuolar size and membrane homeostasis. J. Cell. Biol., 143, 65-79.
13. Ikonomov, O.C., Sbrissa, D., Foti, M., Carpentier, J.L. and Shisheva, A. (2003) PIKfyve controls fluid phase endocytosis but not recycling/degradation of endocytosed receptors or sorting of procathepsin D by regulating multivesicular body morphogenesis. Mol. Biol. Cell., 14, 4581-4591.
14. Ferguson, C.J., Lenk, G.M. and Meisler, M.H. (2009) Defective autophagy in neurons and astrocytes from mice deficient in PI(3,5)P2. Hum. Mol. Genet., 18, 4868-4878.
15. Tsuruta, F., Green, E.M., Rousset, M. and Dolmetsch, R.E. (2009) PIKfyve regulates CaV1.2 degradation and prevents excitotoxic cell death. J. Cell. Biol., 187, 279-294.
16. Zhang, X., Chow, C.Y., Sahenk, Z., Shy, M.E., Meisler, M.H. and Li, J. (2008) Mutation of FIG4 causes a rapidly progressive, asymmetric neuronal degeneration. Brain, 131, 1990-2001.
17. Winters, J.J., Ferguson, C.J., Lenk, G.M., Giger-Mateeva, V.I., Shrager, P., Meisler, M.H. and Giger, R.J. (2011) Congenital CNS hypomylenation in the Fig4 null mouse is rescued by neuronal expression of the PI(3,5)P2 phosphatase Fig4. J. Neurosci., 31, 17736-17751.
18. Nicholson, G., Lenk, G.M., Reddel, S.W., Grant, A.E., Towne, C.F., Ferguson, C.J., Simpson, E., Scheuerle, A., Yasick, M., Hoffman, S. et al. (2011) Distinctive genetic and clinical features of CMT4J: a severe neuropathy caused by mutations in the PI(3,5)P2 phosphatase FIG4. Brain, 134, 1959-1971.
19. Lenk, G.M., Ferguson, C.J., Chow, C.Y., Jin, N., Jones, J.M., Grant, A.E., Zolov, S.N., Winters, J.J., Giger, R.J., Dowling, J.J. et al. (2011) Pathogenic mechanism of the FIG4 mutation responsible for Charcot-Marie-Tooth disease CMT4J. PLoS Genet., 7, e1002104.
20. Lee, Y., Messing, A., Su, M. and Brenner, M. (2008) GFAP promoter elements required for region-specific and astrocyte-specific expression. Glia, 56, 481-493.
21. Zhu, Y., Romero, M.I., Ghosh, P., Ye, Z., Charnay, P., Rushing, E.J., Marth, J.D. and Parada, L.F. (2001) Ablation of NF1 function in neurons induces abnormal development of cerebral cortex and reactive gliosis in the brain. Gene Dev., 15, 859-876.
22. Yu, T., Shakkottai, V.G., Chung, C. and Lieberman, A.P. (2011) Temporal and cell-specific deletion establishes that neuronal Npc1 deficiency is sufficient to mediate neurodegeneration. Hum. Mol. Genet., 20, 4440-4451.
23. Lopez, M.E., Klein, A.D., Dimbil, U.J. and Scott, M.P. (2011) Anatomically defined neuron-based rescue of neurodegenerative Niemann-Pick type C disorder. J. Neurosci., 31, 4367-4378.
24. Dong, X.P., Shen, D., Wang, X., Dawson, T., Li, X., Zhang, Q., Cheng, X., Zhang, Y., Weisman, L.S., Delling, M. and Xu, H. (2010) PI(3,5)P(2) controls membrane trafficking by direct activation of mucolipin Ca(2+) release channels in the endolysosome. Nat. Commun., 1, 10.1038/ncomms1037.
25. Katona, I., Zhang, X., Bai, Y., Shy, M.E., Guo, J., Yan, Q., Hatfield, J., Kupsky, W.J. and Li, J. (2011) Distinct pathogenic processes between Fig4-deficient motor and sensory neurons. Eur. J. Neurosci., 35, 1401-1410.
26. Lloyd-Evans, E. and Platt, F.M. (2011) Lysosomal Ca(2+) homeostasis: role in pathogenesis of lysosomal storage diseases. Cell Calcium, 50, 200-205.
27. Di Giorgio, F.P., Carrasco, M.A., Siao, M.C., Maniatis, T. and Eggan, K.C. (2007) Non-cell autonomous effect of glia on motor neurons in an embryonic stem cell-based ALS model. Nat. Neurosci., 10, 608-614.
28. Nagai, M., Re, D.B., Nagata, T., Chalazonitis, A., Jessell, T.M., Wichterle, H. and Przedborski, S. (2007) Astrocytes expressing ALS-linked mutated SOD1 release factors selectively toxic to motor neurons. Nat. Neurosci., 10, 615-622.
29. Di Giorgio, F.P., Boulting, G.L., Bobrowicz, S. and Eggan, K.C. (2008) Human embryonic stem cell-derived motor neurons are sensitive to the toxic effect of glial cells carrying and ALS-causing mutation. Cell. Stem Cell, 3, 637-648.
30. Marchetto, M.C., Muotri, A.R., Mu, Y., Smith, A.M., Cezar, G.G. and Gage, F.H. (2008) Non-cell-autonomous effect of human SOD1 G37R astrocytes on motor neurons derived from human embryonic stem cells. Cell. Stem Cell, 3, 649-657.
31. Yamanaka, K., Chun, S.J., Boilee, S., Fujimore-Tonou, N., Yamashita, H., Gutmann, D.H., Takahashi, R., Misawa, H. and Cleveland, D.W. (2008) Astrocytes as determinants of disease progression in inherited amyotrophic lateral sclerosis. Nat. Neurosci., 11, 251-253.
32. Papadeas, S.T., Kraig, S.E., O'Banion, C., Lepore, A.C. and Maragakis, N.J. (2011) Astrocytes carrying the superoxide dismutase 1 (SOD1(G93A)) mutation induce wild-type motor neuron degeneration in vivo. Proc. Natl Acad. Sci. USA, 108, 17803-17808.
33. Forss-Petter, S., Danielson, P.E., Catsicas, S., Battenberg, E., Price, J., Nerenberg, M. and Sutcliffe, J.G. (1990) Transgenic mice expressing beta-galactosidase in mature neurons under neuron-specific enolase promoter control. Neuron, 5, 187-197.
34. Mucke, L., Masliah, E., Johnson, W.B., Ruppe, M.D., Alford, M., Rockenstein, E.M., Forss-Petter, S., Pietropaolo, M., Mallory, M. and Abraham, C.R. (1994) Synaptotrophic effects of human amyloid beta protein precursors in the cortex of transgenic mice. Brain Res., 666, 151-167.
35. Race, R.E., Priola, S.A., Bessen, R.A., Ernst, D., Dockter, J., Rall, G.F., Mucke, L., Chesebro, B. and Oldstone, M.B. (1995) Neuron-specific expression of a hamster prion protein minigene in transgenic mice induces susceptibility to hamster scrapie agent. Neuron, 15, 1183-1191.
36. Kearney, J.A., Plummer, N.W., Smith, M.R., Kapur, J., Cummins, T.R., Waxman, S.G., Goldin, A.L. and Meisler, M.H. (2001) A gain-of-function mutation in the sodium channel gene Scn2a results in seizures and behavioral abnormalities. Neuroscience, 102, 307-317.
37. Ferguson, C.J. (2011) Autophagy and cell autonomy in mouse models of PI(3,5)P(2) deficiency. PhD Thesis, University of Michigan, Ann Arbor.
38. Hughes, E.D. and Saunders, T.L. (2011) Gene targeting in embryonic stem cells. In Pease, S. and Saunders, T.L. (eds) Advanced Protocols for Animal Transgenesis: An ISTT Manual. Springer, Berlin, pp. 291-325.
39. Rempe, D., Vangeison, G., Hamilton, J., Li, Y., Jepson, M. and Federoff, H.J. (2006) Synapsin I cre transgene expression in male mice produces germline recombination in progeny. Genesis, 44, 44-49.