Abnormal regulation of TSG101 in mice with spongiform neurodegeneration

Biochimica et Biophysica Acta - Molecular Basis of Disease

Volumn 1792, Issue 10, 2009, Pages 1027-1035

  Jiao, Jian ^a   Sun, Kaihua ^a   Walker, Will P ^a   Bagher, Pooneh ^a   Cota, Christina D ^a   Gunn, Teresa M ^a  

^a Department of Obstetrics Gynecology   (United States)

Author keywords

Endocytic trafficking; Mahogunin Ring Finger 1; MGRN1; Spongiform neurodegeneration; TSG101; Ubiquitination

Indexed keywords

CARRIER PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; TUMOR SUSCEPTIBILITY GENE 101 PROTEIN; UBIQUITIN PROTEIN LIGASE E3;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN SPONGIOSIS; BRAIN TISSUE; CONTROLLED STUDY; EMBRYO; ENDOSOME; GENE MUTATION; GENETIC VARIABILITY; IN VIVO STUDY; LYSOSOME; MOUSE; NERVE DEGENERATION; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN TRANSPORT; UBIQUITINATION; WILD TYPE;

AGING; AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANIMALS; BIOCATALYSIS; BRAIN; CELL LINE; CONSERVED SEQUENCE; DNA-BINDING PROTEINS; ENDOSOMAL SORTING COMPLEXES REQUIRED FOR TRANSPORT; GAG GENE PRODUCTS, HUMAN IMMUNODEFICIENCY VIRUS; HIV-1; HUMANS; MICE; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; NERVE DEGENERATION; RECEPTOR, EPIDERMAL GROWTH FACTOR; SOLUBILITY; TRANSCRIPTION FACTORS; UBIQUITIN-PROTEIN LIGASES; UBIQUITINATION;

MUS;

EID: 70349275158     PISSN: 09254439     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbadis.2009.08.009     Document Type: Article

References (56)

1. Bilello J.A., Pitts O.M., and Hoffman P.M. Characterization of a progressive neurodegenerative disease induced by a temperature-sensitive Moloney murine leukemia virus infection. J. Virol. 59 (1986) 234-241
2. Everall I., Luthert P., and Lantos P. A review of neuronal damage in human immunodeficiency virus infection: its assessment, possible mechanism and relationship to dementia. J. Neuropathol. Exp. Neurol. 52 (1993) 561-566
3. Jacomy H., and Talbot P.J. Vacuolating encephalitis in mice infected by human coronavirus OC43. Virology 315 (2003) 20-33
4. Georgsson G., Palsson P.A., Panitch H., Nathanson N., and Petursson G. The ultrastructure of early visna lesions. Acta Neuropathol. (Berl). 37 (1977) 127-135
5. Baslow M.H. Canavan's spongiform leukodystrophy: a clinical anatomy of a genetic metabolic CNS disease. J. Mol. Neurosci. 15 (2000) 61-69
6. Smith T.W., Anwer U., DeGirolami U., and Drachman D.A. Vacuolar change in Alzheimer's disease. Arch. Neurol. 44 (1987) 1225-1228
7. Iseki E., Li F., and Kosaka K. Close relationship between spongiform change and ubiquitin-positive granular structures in diffuse Lewy body disease. J. Neurol. Sci. 146 (1997) 53-57
8. Filosto M., Tomelleri G., Tonin P., Scarpelli M., Vattemi G., Rizzuto N., Padovani A., and Simonati A. Neuropathology of mitochondrial diseases. Biosci. Rep. 27 (2007) 23-30
9. Chow C.Y., Zhang Y., Dowling J.J., Jin N., Adamska M., Shiga K., Szigeti K., Shy M.E., Li J., Zhang X., Lupski J.R., Weisman L.S., and Meisler M.H. Mutation of FIG4 causes neurodegeneration in the pale tremor mouse and patients with CMT4J. Nature 448 (2007) 68-72
10. 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., Meisler M.H., and Weisman L.S. Loss of Vac14, a regulator of the signaling lipid phosphatidylinositol 3,5-bisphosphate, results in neurodegeneration in mice. Proc. Natl. Acad. Sci. U. S. A. 104 (2007) 17518-17523
11. He L., Lu X.Y., Jolly A.F., Eldridge A.G., Watson S.J., Jackson P.K., Barsh G.S., and Gunn T.M. Spongiform degeneration in mahoganoid mutant mice. Science 299 (2003) 710-712
12. 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. A biochemical function for attractin in agouti-induced pigmentation and obesity. Nat. Genet. 27 (2001) 40-47
13. Neusch C., Rozengurt N., Jacobs R.E., Lester H.A., and Kofuji P. Kir4.1 potassium channel subunit is crucial for oligodendrocyte development and in vivo myelination. J. Neurosci. 21 (2001) 5429-5438
14. Melov S., Schneider J.A., Day B.J., Hinerfeld D., Coskun P., Mirra S.S., Crapo J.D., and Wallace D.C. A novel neurological phenotype in mice lacking mitochondrial manganese superoxide dismutase. Nat. Genet. 18 (1998) 159-163
15. Lebovitz R.M., Zhang H., Vogel H., Cartwright Jr. J., Dionne L., Lu N., Huang S., and Matzuk M.M. Neurodegeneration, myocardial injury, and perinatal death in mitochondrial superoxide dismutase-deficient mice. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 9782-9787
16. Gissen P., Johnson C.A., Morgan N.V., Stapelbroek J.M., Forshew T., Cooper W.N., McKiernan P.J., Klomp L.W., Morris A.A., Wraith J.E., McClean P., Lynch S.A., Thompson R.J., Lo B., Quarrell O.W., Di Rocco M., Trembath R.C., Mandel H., Wali S., Karet F.E., Knisely A.S., Houwen R.H., Kelly D.A., and Maher E.R. Mutations in VPS33B, encoding a regulator of SNARE-dependent membrane fusion, cause arthrogryposis-renal dysfunction-cholestasis (ARC) syndrome. Nat. Genet. 36 (2004) 400-404
17. 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., and Stenmark H. ESCRTs and Fab1 regulate distinct steps of autophagy. Curr. Biol. 17 (2007) 1817-1825
18. Metzler M., Legendre-Guillemin V., Gan L., Chopra V., Kwok A., McPherson P.S., and Hayden M.R. HIP1 functions in clathrin-mediated endocytosis through binding to clathrin and adaptor protein 2. J. Biol. Chem. 276 (2001) 39271-39276
19. Nixon R.A., and Cataldo A.M. Lysosomal system pathways: genes to neurodegeneration in Alzheimer's disease. J. Alzheimers Dis. 9 (2006) 277-289
20. Parkinson N., Ince P.G., Smith M.O., Highley R., Skibinski G., Andersen P.M., Morrison K.E., Pall H.S., Hardiman O., Collinge J., Shaw P.J., and Fisher E.M. ALS phenotypes with mutations in CHMP2B (charged multivesicular body protein 2B). Neurology 67 (2006) 1074-1077
21. Stein M.P., Dong J., and Wandinger-Ness A. Rab proteins and endocytic trafficking: potential targets for therapeutic intervention. Adv. Drug Deliv. Rev. 55 (2003) 1421-1437
22. Skibinski G., Parkinson N.J., Brown J.M., Chakrabarti L., Lloyd S.L., Hummerich H., Nielsen J.E., Hodges J.R., Spillantini M.G., Thusgaard T., Brandner S., Brun A., Rossor M.N., Gade A., Johannsen P., Sorensen S.A., Gydesen S., Fisher E.M., and Collinge J. Mutations in the endosomal ESCRTIII-complex subunit CHMP2B in frontotemporal dementia. Nat. Genet. 37 (2005) 806-808
23. Lee J.A., Beigneux A., Ahmad S.T., Young S.G., and Gao F.B. ESCRT-III dysfunction causes autophagosome accumulation and neurodegeneration. Curr. Biol. 17 (2007) 1561-1567
24. Bronfman F.C., Escudero C.A., Weis J., and Kruttgen A. Endosomal transport of neurotrophins: roles in signaling and neurodegenerative diseases. Dev. Neurobiol. 67 (2007) 1183-1203
25. Piper R.C., and Katzmann D.J. Biogenesis and function of multivesicular bodies. Annu. Rev. Cell Dev. Biol. 23 (2007) 519-547
26. Hershko A., and Ciechanover A. The ubiquitin system. Annu. Rev. Biochem. 67 (1998) 425-479
27. Urbe S. Ubiquitin and endocytic protein sorting. Essays Biochem. 41 (2005) 81-98
28. Hurley J.H. ESCRT complexes and the biogenesis of multivesicular bodies. Curr. Opin. Cell Biol. (2008)
29. Katzmann D.J., Odorizzi G., and Emr S.D. Receptor downregulation and multivesicular-body sorting. Nat. Rev. Mol. Cell Biol. 3 (2002) 893-905
30. Williams R.L., and Urbe S. The emerging shape of the ESCRT machinery. Nat. Rev. Mol. Cell. Biol. 8 (2007) 355-368
31. Garrus J.E., von Schwedler U.K., Pornillos O.W., Morham S.G., Zavitz K.H., Wang H.E., Wettstein D.A., Stray K.M., Cote M., Rich R.L., Myszka D.G., and Sundquist W.I. Tsg101 and the vacuolar protein sorting pathway are essential for HIV-1 budding. Cell 107 (2001) 55-65
32. Demirov D.G., Ono A., Orenstein J.M., and Freed E.O. Overexpression of the N-terminal domain of TSG101 inhibits HIV-1 budding by blocking late domain function. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 955-960
33. Blot V., Perugi F., Gay B., Prevost M.C., Briant L., Tangy F., Abriel H., Staub O., Dokhelar M.C., and Pique C. Nedd4.1-mediated ubiquitination and subsequent recruitment of Tsg101 ensure HTLV-1 Gag trafficking towards the multivesicular body pathway prior to virus budding. J. Cell Sci. 117 (2004) 2357-2367
34. Martin-Serrano J., Zang T., and Bieniasz P.D. HIV-1 and Ebola virus encode small peptide motifs that recruit Tsg101 to sites of particle assembly to facilitate egress. Nat. Med. 7 (2001) 1313-1319
35. Luttge B.G., Shehu-Xhilaga M., Demirov D.G., Adamson C.S., Soheilian F., Nagashima K., Stephen A.G., Fisher R.J., and Freed E.O. Molecular characterization of feline immunodeficiency virus budding. J. Virol. (2007)
36. Patton G.S., Morris S.A., Chung W., Bieniasz P.D., and McClure M.O. Identification of domains in gag important for prototypic foamy virus egress. J. Virol. 79 (2005) 6392-6399
37. Sun K., Johnson B.S., and Gunn T.M. Mitochondrial dysfunction precedes neurodegeneration in Mahogunin (Mgrn1) mutant mice. Neurobiol. Aging 28 (2007) 1840-1852
38. Miller K.A., Gunn T.M., Carrasquillo M.M., Lamoreux M.L., Galbraith D.B., and Barsh G.S. Genetic studies of the mouse mutations mahogany and mahoganoid. Genetics 146 (1997) 1407-1415
39. Cota C.D., Bagher P., Pelc P., Smith C.O., Bodner C.R., and Gunn T.M. Mice with mutations in Mahogunin ring finger-1 (Mgrn1) exhibit abnormal patterning of the left-right axis. Dev. Dyn. 235 (2006) 3438-3447
40. Kim B.Y., Olzmann J.A., Barsh G.S., Chin L.S., and Li L. Spongiform neurodegeneration-associated E3 ligase Mahogunin ubiquitylates TSG101 and regulates endosomal trafficking. Mol. Biol. Cell 18 (2007) 1129-1142
41. Bergink S., Salomons F.A., Hoogstraten D., Groothuis T.A., de Waard H., Wu J., Yuan L., Citterio E., Houtsmuller A.B., Neefjes J., Hoeijmakers J.H., Vermeulen W., and Dantuma N.P. DNA damage triggers nucleotide excision repair-dependent monoubiquitylation of histone H2A. Genes Dev. 20 (2006) 1343-1352
42. Ako-Adjei D., Johnson M.C., and Vogt V.M. The retroviral capsid domain dictates virion size, morphology, and coassembly of gag into virus-like particles. J. Virol. 79 (2005) 13463-13472
43. Bishop N., and Woodman P. ATPase-defective mammalian VPS4 localizes to aberrant endosomes and impairs cholesterol trafficking. Mol. Biol. Cell 11 (2000) 227-239
44. Amit I., Yakir L., Katz M., Zwang Y., Marmor M.D., Citri A., Shtiegman K., Alroy I., Tuvia S., Reiss Y., Roubini E., Cohen M., Wides R., Bacharach E., Schubert U., and Yarden Y. Tal, a Tsg101-specific E3 ubiquitin ligase, regulates receptor endocytosis and retrovirus budding. Genes Dev. 18 (2004) 1737-1752
45. McDonald B., and Martin-Serrano J. Regulation of Tsg101 expression by the steadiness box: a role of Tsg101-associated ligase. Mol. Biol. Cell 19 (2008) 754-763
46. Pornillos O., Higginson D.S., Stray K.M., Fisher R.D., Garrus J.E., Payne M., He G.P., Wang H.E., Morham S.G., and Sundquist W.I. HIV Gag mimics the Tsg101-recruiting activity of the human Hrs protein. J. Cell Biol. 162 (2003) 425-434
47. Itahana K., Mao H., Jin A., Itahana Y., Clegg H.V., Lindstrom M.S., Bhat K.P., Godfrey V.L., Evan G.I., and Zhang Y. Targeted inactivation of Mdm2 RING finger E3 ubiquitin ligase activity in the mouse reveals mechanistic insights into p53 regulation. Cancer Cell. 12 (2007) 355-366
48. Li L., Liao J., Ruland J., Mak T.W., and Cohen S.N. A TSG101/MDM2 regulatory loop modulates MDM2 degradation and MDM2/p53 feedback control. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 1619-1624
49. Cheng T.H., and Cohen S.N. Human MDM2 isoforms translated differentially on constitutive versus p53-regulated transcripts have distinct functions in the p53/MDM2 and TSG101/MDM2 feedback control loops. Mol. Cell. Biol. 27 (2007) 111-119
50. Longva K.E., Blystad F.D., Stang E., Larsen A.M., Johannessen L.E., and Madshus I.H. Ubiquitination and proteasomal activity is required for transport of the EGF receptor to inner membranes of multivesicular bodies. J. Cell Biol. 156 (2002) 843-854
51. Yokouchi M., Kondo T., Houghton A., Bartkiewicz M., Horne W.C., Zhang H., Yoshimura A., and Baron R. Ligand-induced ubiquitination of the epidermal growth factor receptor involves the interaction of the c-Cbl RING finger and UbcH7. J. Biol. Chem. 274 (1999) 31707-31712
52. Ettenberg S.A., Magnifico A., Cuello M., Nau M.M., Rubinstein Y.R., Yarden Y., Weissman A.M., and Lipkowitz S. Cbl-b-dependent coordinated degradation of the epidermal growth factor receptor signaling complex. J. Biol. Chem. 276 (2001) 27677-27684
53. Cha Y.K., Kim Y.H., Ahn Y.H., and Koh J.Y. Epidermal growth factor induces oxidative neuronal injury in cortical culture. J. Neurochem. 75 (2000) 298-303
54. Doyotte A., Russell M.R., Hopkins C.R., and Woodman P.G. Depletion of TSG101 forms a mammalian "Class E" compartment: a multicisternal early endosome with multiple sorting defects. J. Cell Sci. 118 (2005) 3003-3017
55. Katzmann D.J., Stefan C.J., Babst M., and Emr S.D. Vps27 recruits ESCRT machinery to endosomes during MVB sorting. J. Cell Biol. 162 (2003) 413-423
56. Jin N., Chow C.Y., Liu L., Zolov S.N., Bronson R., Davisson M., Petersen J.L., Zhang Y., Park S., Duex J.E., Goldowitz D., Meisler M.H., and Weisman L.S. 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 (2008) 3221-3234