La FAM fatale: USP9X in development and disease

Cellular and Molecular Life Sciences

Volumn 72, Issue 11, 2015, Pages 2075-2089

  Murtaza, Mariyam ^a   Jolly, Lachlan A ^b   Gecz, Jozef ^b   Wood, Stephen A ^a  

^a GRIFFITH UNIVERSITY   (Australia)

^b UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

Embryo; Fat facets; Stem cells; Ubiquitin

Indexed keywords

DEUBIQUITINASE; UBIQUITIN THIOLESTERASE; USP9X PROTEIN, HUMAN;

ANIMAL; APOPTOSIS; AUTOIMMUNE DISEASE; CELL POLARITY; DEGENERATIVE DISEASE; DROSOPHILA; EMBRYO DEVELOPMENT; GENE EXPRESSION REGULATION; GENETICS; HUMAN; METABOLISM; NEOPLASM; NERVOUS SYSTEM DEVELOPMENT; PROTEIN PROCESSING; PROTEIN TRANSPORT; UBIQUITINATION;

ANIMALS; APOPTOSIS; AUTOIMMUNE DISEASES; CELL POLARITY; DROSOPHILA; EMBRYONIC DEVELOPMENT; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HUMANS; NEOPLASMS; NEURODEGENERATIVE DISEASES; NEUROGENESIS; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN TRANSPORT; UBIQUITIN THIOLESTERASE; UBIQUITIN-SPECIFIC PROTEASES; UBIQUITINATION;

EID: 84939987112     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-015-1851-0     Document Type: Review

References (121)

1. Hershko A, Ciechanover A (1998) The ubiquitin system. Annu Rev Biochem 67:425-479
2. Kerscher O, Felberbaum R, Hochstrasser M (2006) Modification of proteins by ubiquitin and ubiquitin-like proteins. Annu Rev Cell Dev Biol 22:159-180
3. Nijman SM, Luna-Vargas MP, Velds A, Brummelkamp TR, Dirac AM et al (2005) A genomic and functional inventory of deubiquitinating enzymes. Cell 123:773-786
4. Amerik AY, Hochstrasser M (2004) Mechanism and function of deubiquitinating enzymes. Biochim Biophys Acta 1695:189-207
5. Aberle H, Bauer A, Stappert J, Kispert A, Kemler R (1997) beta-catenin is a target for the ubiquitin-proteasome pathway. EMBO J 16:3797-3804
6. 2-regulated prolyl hydroxylation. Science 292:468-472
7. Grou CP, Francisco T, Rodrigues TA, Freitas MO, Pinto MP et al (2012) Identification of ubiquitin-specific protease 9X (USP9X) as a deubiquitinase acting on ubiquitin-peroxin 5 (PEX5) thioester conjugate. J Biol Chem 287:12815-12827
8. Al-Hakim AK, Zagorska A, Chapman L, Deak M, Peggie M et al (2008) Control of AMPK-related kinases by USP9X and atypical Lys(29)/Lys(33)-linked polyubiquitin chains. Biochem J 411:249-260
9. Dupont S, Mamidi A, Cordenonsi M, Montagner M, Zacchigna L et al (2009) FAM/USP9x, a deubiquitinating enzyme essential for TGFbeta signaling, controls Smad4 monoubiquitination. Cell 136:123-135
10. Marx C, Held JM, Gibson BW, Benz CC (2010) ErbB2 trafficking and degradation associated with K48 and K63 polyubiquitination. Cancer Res 70:3709-3717
11. Mouchantaf R, Azakir BA, McPherson PS, Millard SM, Wood SA et al (2006) The ubiquitin ligase itch is auto-ubiquitylated in vivo and in vitro but is protected from degradation by interacting with the deubiquitylating enzyme FAM/USP9X. J Biol Chem 281:38738-38747
12. Taya S, Yamamoto T, Kano K, Kawano Y, Iwamatsu A et al (1998) The Ras target AF-6 is a substrate of the fam deubiquitinating enzyme. J Cell Biol 142:1053-1062
13. Vong QP, Cao K, Li HY, Iglesias PA, Zheng Y (2005) Chromosome alignment and segregation regulated by ubiquitination of survivin. Science 310:1499-1504
14. Khut PY, Tucker B, Lardelli M, Wood SA (2007) Evolutionary and expression analysis of the zebrafish deubiquitylating enzyme, usp9. Zebrafish 4:95-101
15. Fischer-Vize JA, Rubin GM, Lehmann R (1992) The fat facets gene is required for Drosophila eye and embryo development. Development 116:985-1000
16. Chen X, Overstreet E, Wood SA, Fischer JA (2000) On the conservation of function of the Drosophila fat facets deubiquitinating enzyme and Fam, its mouse homolog. Dev Genes Evol 210:603-610
17. Wood SA, Pascoe WS, Ru K, Yamada T, Hirchenhain J et al (1997) Cloning and expression analysis of a novel mouse gene with sequence similarity to the Drosophila fat facets gene. Mech Dev 63:29-38
18. Homan CC, Kumar R, Nguyen LS, Haan E, Raymond FL et al (2014) Mutations in USP9X Are Associated with X-Linked Intellectual Disability and Disrupt Neuronal Cell Migration and Growth. Am J Hum Genet 94:470-478
19. Petrovski S, Wang Q, Heinzen EL, Allen AS, Goldstein DB (2013) Genic intolerance to functional variation and the interpretation of personal genomes. PLoS Genet 9:e1003709
20. Cooper GM, Stone EA, Asimenos G, Green ED, Batzoglou S et al (2005) Distribution and intensity of constraint in mammalian genomic sequence. Genome Res 15:901-913
21. Jolly LA, Taylor V, Wood SA (2009) USP9X enhances the polarity and self-renewal of embryonic stem cell-derived neural progenitors. Mol Biol Cell 20:2015-2029
22. Murray RZ, Jolly LA, Wood SA (2004) The FAM deubiquitylating enzyme localizes to multiple points of protein trafficking in epithelia, where it associates with E-cadherin and beta-catenin. Mol Biol Cell 15:1591-1599
23. Theard D, Labarrade F, Partisani M, Milanini J, Sakagami H et al (2010) USP9x-mediated deubiquitination of EFA6 regulates de novo tight junction assembly. EMBO J 29:1499-1509
24. Schwickart M, Huang X, Lill JR, Liu J, Ferrando R et al (2010) Deubiquitinase USP9X stabilizes MCL1 and promotes tumour cell survival. Nature 463:103-107
25. Trinkle-Mulcahy L, Boulon S, Lam YW, Urcia R, Boisvert FM et al (2008) Identifying specific protein interaction partners using quantitative mass spectrometry and bead proteomes. J Cell Biol 183:223-239
26. Urbe S, Liu H, Hayes SD, Heride C, Rigden DJ et al (2012) Systematic survey of deubiquitinase localization identifies USP21 as a regulator of centrosome- and microtubule-associated functions. Mol Biol Cell 23:1095-1103
27. Xu Z, Xia B, Gong Q, Bailey J, Groves B et al (2010) Identification of a deubiquitinating enzyme as a novel AGS3-interacting protein. PLoS One 5:e9725
28. Hicke L (2001) Protein regulation by monoubiquitin. Nat Rev Mol Cell Biol 2:195-201
29. Hicke L, Dunn R (2003) Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu Rev Cell Dev Biol 19:141-172
30. Millard SM, Wood SA (2006) Riding the DUBway: regulation of protein trafficking by deubiquitylating enzymes. J Cell Biol 173:463-468
31. Cadavid AL, Ginzel A, Fischer JA (2000) The function of the Drosophila fat facets deubiquitinating enzyme in limiting photoreceptor cell number is intimately associated with endocytosis. Development 127:1727-1736
32. Chen X, Zhang B, Fischer JA (2002) A specific protein substrate for a deubiquitinating enzyme: liquid facets is the substrate of Fat facets. Genes Dev 16:289-294
33. Overstreet E, Fitch E, Fischer JA (2004) Fat facets and Liquid facets promote Delta endocytosis and Delta signaling in the signaling cells. Development 131:5355-5366
34. Wang W, Struhl G (2004) Drosophila Epsin mediates a select endocytic pathway that DSL ligands must enter to activate Notch. Development 131:5367-5380
35. 2+-dependent decrease of protein ubiquitination at synapses. Proc Natl Acad Sci USA 100:14908-14913
36. Angers A, Ramjaun AR, McPherson PS (2004) The HECT domain ligase itch ubiquitinates endophilin and localizes to the trans-Golgi network and endosomal system. J Biol Chem 279:11471-11479
37. Azakir BA, Angers A (2009) Reciprocal regulation of the ubiquitin ligase Itch and the epidermal growth factor receptor signaling. Cell Signal 21:1326-1336
38. Magnifico A, Ettenberg S, Yang C, Mariano J, Tiwari S et al (2003) WW domain HECT E3s target Cbl RING finger E3s for proteasomal degradation. J Biol Chem 278:43169-43177
39. Choe EA, Liao L, Zhou JY, Cheng D, Duong DM et al (2007) Neuronal morphogenesis is regulated by the interplay between cyclin-dependent kinase 5 and the ubiquitin ligase mind bomb 1. J Neurosci 27:9503-9512
40. Tseng LC, Zhang C, Cheng CM, Xu H, Hsu CH et al (2014) New classes of mind bomb-interacting proteins identified from yeast two-hybrid screens. PLoS One 9:e93394
41. Kwon DY, Dimitriadi M, Terzic B, Cable C, Hart AC et al (2013) The E3 ubiquitin ligase mind bomb 1 ubiquitinates and promotes the degradation of survival of motor neuron protein. Mol Biol Cell 24:1863-1871
42. Han KJ, Foster DG, Zhang NY, Kanisha K, Dzieciatkowska M et al (2012) Ubiquitin-specific protease 9x deubiquitinates and stabilizes the spinal muscular atrophy protein-survival motor neuron. J Biol Chem 287:43741-43752
43. Zallen JA (2007) Planar polarity and tissue morphogenesis. Cell 129:1051-1063
44. Strutt H, Searle E, Thomas-Macarthur V, Brookfield R, Strutt D (2013) A Cul-3-BTB ubiquitylation pathway regulates junctional levels and asymmetry of core planar polarity proteins. Development 140:1693-1702
45. Luton F, Klein S, Chauvin JP, Le Bivic A, Bourgoin S et al (2004) EFA6, exchange factor for ARF6, regulates the actin cytoskeleton and associated tight junction in response to E-cadherin engagement. Mol Biol Cell 15:1134-1145
46. Kanai-Azuma M, Mattick JS, Kaibuchi K, Wood SA (2000) Co-localization of FAM and AF-6, the mammalian homologues of Drosophila faf and canoe, in mouse eye development. Mech Dev 91:383-386
47. Pantaleon M, Kanai-Azuma M, Mattick JS, Kaibuchi K, Kaye PL et al (2001) FAM deubiquitylating enzyme is essential for preimplantation mouse embryo development. Mech Dev 109:151-160
48. Assemat E, Bazellieres E, Pallesi-Pocachard E, Le Bivic A, Massey-Harroche D (2008) Polarity complex proteins. Biochim Biophys Acta 1778:614-630
49. Al-Hakim AK, Goransson O, Deak M, Toth R, Campbell DG et al (2005) 14-3-3 cooperates with LKB1 to regulate the activity and localization of QSK and SIK. J Cell Sci 118:5661-5673
50. Baas AF, Smit L, Clevers H (2004) LKB1 tumor suppressor protein: PARtaker in cell polarity. Trends Cell Biol 14:312-319
51. Ryoo HD, Bergmann A, Gonen H, Ciechanover A, Steller H (2002) Regulation of Drosophila IAP1 degradation and apoptosis by reaper and ubcD1. Nat Cell Biol 4:432-438
52. Wing JP, Schreader BA, Yokokura T, Wang Y, Andrews PS et al (2002) Drosophila Morgue is an F box/ubiquitin conjugase domain protein important for grim-reaper mediated apoptosis. Nat Cell Biol 4:451-456
53. Nagai H, Noguchi T, Homma K, Katagiri K, Takeda K et al (2009) Ubiquitin-like sequence in ASK1 plays critical roles in the recognition and stabilization by USP9X and oxidative stress-induced cell death. Mol Cell 36:805-818
54. Huntwork-Rodriguez S, Wang B, Watkins T, Ghosh AS, Pozniak CD et al (2013) JNK-mediated phosphorylation of DLK suppresses its ubiquitination to promote neuronal apoptosis. J Cell Biol 202:747-763
55. Arbour N, Vanderluit JL, Le Grand JN, Jahani-Asl A, Ruzhynsky VA et al (2008) Mcl-1 is a key regulator of apoptosis during CNS development and after DNA damage. J Neurosci 28:6068-6078
56. Dzhagalov I, St John A, He YW (2007) The antiapoptotic protein Mcl-1 is essential for the survival of neutrophils but not macrophages. Blood 109:1620-1626
57. Opferman JT, Letai A, Beard C, Sorcinelli MD, Ong CC et al (2003) Development and maintenance of B and T lymphocytes requires antiapoptotic MCL-1. Nature 426:671-676
58. Zhang C, Cai TY, Zhu H, Yang LQ, Jiang H et al (2011) Synergistic antitumor activity of gemcitabine and ABT-737 in vitro and in vivo through disrupting the interaction of USP9X and Mcl-1. Mol Cancer Ther 10:1264-1275
59. Sun H, Kapuria V, Peterson LF, Fang D, Bornmann WG et al (2011) Bcr-Abl ubiquitination and Usp9x inhibition block kinase signaling and promote CML cell apoptosis. Blood 117:3151-3162
60. Aveic S, Pigazzi M, Basso G (2011) BAG1: the guardian of anti-apoptotic proteins in acute myeloid leukemia. PLoS One 6:e26097
61. Mita AC, Mita MM, Nawrocki ST, Giles FJ (2008) Survivin: key regulator of mitosis and apoptosis and novel target for cancer therapeutics. Clin Cancer Res 14:5000-5005
62. Naik E, Webster JD, DeVoss J, Liu J, Suriben R et al (2014) Regulation of proximal T cell receptor signaling and tolerance induction by deubiquitinase Usp9X. J Exp Med 211:1947-1955
63. Stinchfield MJ, Takaesu NT, Quijano JC, Castillo AM, Tiusanen N et al (2012) Fat facets deubiquitylation of Medea/Smad4 modulates interpretation of a Dpp morphogen gradient. Development 139:2721-2729
64. Stegeman S, Jolly LA, Premarathne S, Gecz J, Richards LJ et al (2013) Loss of Usp9x disrupts cortical architecture, hippocampal development and TGFbeta-mediated axonogenesis. PLoS One 8:e68287
65. Xie Y, Avello M, Schirle M, McWhinnie E, Feng Y et al (2013) Deubiquitinase FAM/USP9X interacts with the E3 ubiquitin ligase SMURF1 protein and protects it from ligase activity-dependent self-degradation. J Biol Chem 288:2976-2985
66. Vigano MA, Lamartine J, Testoni B, Merico D, Alotto D et al (2006) New p63 targets in keratinocytes identified by a genome-wide approach. EMBO J 25:5105-5116
67. Wei CL, Wu Q, Vega VB, Chiu KP, Ng P et al (2006) A global map of p53 transcription-factor binding sites in the human genome. Cell 124:207-219
68. Shen G, Lin Y, Yang X, Zhang J, Xu Z et al (2014) MicroRNA-26b inhibits epithelial-mesenchymal transition in hepatocellular carcinoma by targeting USP9X. BMC Cancer 14:393
69. Ramalho-Santos M, Yoon S, Matsuzaki Y, Mulligan RC, Melton DA (2002) "Stemness": transcriptional profiling of embryonic and adult stem cells. Science 298:597-600
70. Blanpain C, Lowry WE, Geoghegan A, Polak L, Fuchs E (2004) Self-renewal, multipotency, and the existence of two cell populations within an epithelial stem cell niche. Cell 118:635-648
71. Ivanova NB, Dimos JT, Schaniel C, Hackney JA, Moore KA et al (2002) A stem cell molecular signature. Science 298:601-604
72. Van Hoof D, Passier R, Ward-Van Oostwaard D, Pinkse MW, Heck AJ et al (2006) A quest for human and mouse embryonic stem cell-specific proteins. Mol Cell Proteomics 5:1261-1273
73. Li QR, Xing XB, Chen TT, Li RX, Dai J et al (2011) Large scale phosphoproteome profiles comprehensive features of mouse embryonic stem cells. Mol Cell Proteomics 10(M110):001750
74. Cox JL, Wilder PJ, Gilmore JM, Wuebben EL, Washburn MP et al (2013) The SOX2-interactome in brain cancer cells identifies the requirement of MSI2 and USP9X for the growth of brain tumor cells. PLoS One 8:e62857
75. van den Berg DL, Snoek T, Mullin NP, Yates A, Bezstarosti K et al (2010) An Oct4-centered protein interaction network in embryonic stem cells. Cell Stem Cell 6:369-381
76. Agrawal P, Chen YT, Schilling B, Gibson BW, Hughes RE (2012) Ubiquitin-specific peptidase 9, X-linked (USP9X) modulates activity of mammalian target of rapamycin (mTOR). J Biol Chem 287:21164-21175
77. Bao H, Reist NE, Zhang B (2008) The Drosophila epsin 1 is required for ubiquitin-dependent synaptic growth and function but not for synaptic vesicle recycling. Traffic 9:2190-2205
78. Lee S, Wang JW, Yu W, Lu B (2012) Phospho-dependent ubiquitination and degradation of PAR-1 regulates synaptic morphology and tau-mediated Abeta toxicity in Drosophila. Nat Commun 3:1312
79. Tarpey PS, Smith R, Pleasance E, Whibley A, Edkins S et al (2009) A systematic, large-scale resequencing screen of X-chromosome coding exons in mental retardation. Nat Genet 41:535-543
80. des Portes V, Pinard JM, Billuart P, Vinet MC, Koulakoff A et al (1998) A novel CNS gene required for neuronal migration and involved in X-linked subcortical laminar heterotopia and lissencephaly syndrome. Cell 92:51-61
81. Gleeson JG, Lin PT, Flanagan LA, Walsh CA (1999) Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron 23:257-271
82. Friocourt G, Kappeler C, Saillour Y, Fauchereau F, Rodriguez MS et al (2005) Doublecortin interacts with the ubiquitin protease DFFRX, which associates with microtubules in neuronal processes. Mol Cell Neurosci 28:153-164
83. Deuel TA, Liu JS, Corbo JC, Yoo SY, Rorke-Adams LB et al (2006) Genetic interactions between doublecortin and doublecortin-like kinase in neuronal migration and axon outgrowth. Neuron 49:41-53
84. Tanaka T, Koizumi H, Gleeson JG (2006) The doublecortin and doublecortin-like kinase 1 genes cooperate in murine hippocampal development. Cereb Cortex 16(Suppl 1):i69-i73
85. Brett M, McPherson J, Zang ZJ, Lai A, Tan ES et al (2014) Massively parallel sequencing of patients with intellectual disability, congenital anomalies and/or autism spectrum disorders with a targeted gene panel. PLoS One 9:e93409
86. Rott R, Szargel R, Haskin J, Bandopadhyay R, Lees AJ et al (2011) alpha-Synuclein fate is determined by USP9X-regulated monoubiquitination. Proc Natl Acad Sci USA 108:18666-18671
87. Engelender S (2012) alpha-Synuclein fate: proteasome or autophagy? Autophagy 8:418-420
88. Kaltenbach LS, Romero E, Becklin RR, Chettier R, Bell R et al (2007) Huntingtin interacting proteins are genetic modifiers of neurodegeneration. PLoS Genet 3:e82
89. Luise C, Capra M, Donzelli M, Mazzarol G, Jodice MG et al (2011) An atlas of altered expression of deubiquitinating enzymes in human cancer. PLoS One 6:e15891
90. Forbes SA, Bindal N, Bamford S, Cole C, Kok CY et al (2011) COSMIC: mining complete cancer genomes in the Catalogue of Somatic Mutations in Cancer. Nucleic Acids Res 39:D945-D950
91. Oncomine Research Edition Database. https://www.oncomine.org
92. Wang S, Kollipara RK, Srivastava N, Li R, Ravindranathan P et al (2014) Ablation of the oncogenic transcription factor ERG by deubiquitinase inhibition in prostate cancer. Proc Natl Acad Sci USA 111:4251-4256
93. Nadiminty N, Lou W, Lee SO, Mehraein-Ghomi F, Kirk JS et al (2006) Prostate-specific antigen modulates genes involved in bone remodeling and induces osteoblast differentiation of human osteosarcoma cell line SaOS-2. Clin Cancer Res 12:1420-1430
94. Peng J, Hu Q, Liu W, He X, Cui L et al (2013) USP9X expression correlates with tumor progression and poor prognosis in esophageal squamous cell carcinoma. Diagn Pathol 8:177
95. Perez-Mancera PA, Rust AG, van der Weyden L, Kristiansen G, Li A et al (2012) The deubiquitinase USP9X suppresses pancreatic ductal adenocarcinoma. Nature 486:266-270
96. Oosterkamp HM, Hijmans EM, Brummelkamp TR, Canisius S, Wessels LF et al (2014) USP9X downregulation renders breast cancer cells resistant to tamoxifen. Cancer Res 74:3810-3820
97. Rivlin N, Katz S, Doody M, Sheffer M, Horesh S et al (2014) Rescue of embryonic stem cells from cellular transformation by proteomic stabilization of mutant p53 and conversion into WT conformation. Proc Natl Acad Sci USA 111:7006-7011
98. Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO et al (2012) The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov 2:401-404
99. Gao J, Aksoy BA, Dogrusoz U, Dresdner G, Gross B et al (2013) Integrative analysis of complex cancer genomics and clinical profiles using the cBioPortal. Sci Signal 6:pl1
100. ICGC IPTo (2013) Mutational landscape of gingivo-buccal oral squamous cell carcinoma reveals new recurrently-mutated genes and molecular subgroups. Nat Commun 4:2873
101. Beroukhim R, Mermel CH, Porter D, Wei G, Raychaudhuri S et al (2010) The landscape of somatic copy-number alteration across human cancers. Nature 463:899-905
102. Campbell KJ, Bath ML, Turner ML, Vandenberg CJ, Bouillet P et al (2010) Elevated Mcl-1 perturbs lymphopoiesis, promotes transformation of hematopoietic stem/progenitor cells, and enhances drug resistance. Blood 116:3197-3207
103. Glaser SP, Lee EF, Trounson E, Bouillet P, Wei A et al (2012) Anti-apoptotic Mcl-1 is essential for the development and sustained growth of acute myeloid leukemia. Genes Dev 26:120-125
104. Peddaboina C, Jupiter D, Fletcher S, Yap JL, Rai A et al (2012) The downregulation of Mcl-1 via USP9X inhibition sensitizes solid tumors to Bcl-xl inhibition. BMC Cancer 12:541
105. Trivigno D, Essmann F, Huber SM, Rudner J (2012) Deubiquitinase USP9x confers radioresistance through stabilization of Mcl-1. Neoplasia 14:893-904
106. Mazur PK, Gruner BM, Nakhai H, Sipos B, Zimber-Strobl U et al (2010) Identification of epidermal Pdx1 expression discloses different roles of Notch1 and Notch2 in murine Kras(G12D)-induced skin carcinogenesis in vivo. PLoS One 5:e13578
107. Kapuria V, Peterson LF, Fang D, Bornmann WG, Talpaz M et al (2010) Deubiquitinase inhibition by small-molecule WP1130 triggers aggresome formation and tumor cell apoptosis. Cancer Res 70:9265-9276
108. Flavell SW, Kim TK, Gray JM, Harmin DA, Hemberg M et al (2008) Genome-wide analysis of MEF2 transcriptional program reveals synaptic target genes and neuronal activity-dependent polyadenylation site selection. Neuron 60:1022-1038
109. Sato T, Kanai Y, Noma T, Kanai-Azuma M, Taya S et al (2004) A close correlation in the expression patterns of Af-6 and Usp9x in Sertoli and granulosa cells of mouse testis and ovary. Reproduction 128:583-594
110. Park Y, Jin HS, Liu YC (2013) Regulation of T cell function by the ubiquitin-specific protease USP9X via modulating the Carma1-Bcl10-Malt1 complex. Proc Natl Acad Sci USA 110:9433-9438
111. Taya S, Yamamoto T, Kanai-Azuma M, Wood SA, Kaibuchi K (1999) The deubiquitinating enzyme Fam interacts with and stabilizes beta-catenin. Genes Cells 4:757-767
112. Nathan JA, Sengupta S, Wood SA, Admon A, Markson G et al (2008) The ubiquitin E3 ligase MARCH7 is differentially regulated by the deubiquitylating enzymes USP7 and USP9X. Traffic 9:1130-1145
113. Liu N, Dansereau DA, Lasko P (2003) Fat facets interacts with vasa in the Drosophila pole plasm and protects it from degradation. Curr Biol 13:1905-1909
114. Zheng X, Zhai B, Koivunen P, Shin SJ, Lu G et al (2014) Prolyl hydroxylation by EglN2 destabilizes FOXO3a by blocking its interaction with the USP9x deubiquitinase. Genes Dev 28:1429-1444
115. Joshi P, Greco TM, Guise AJ, Luo Y, Yu F et al (2013) The functional interactome landscape of the human histone deacetylase family. Mol Syst Biol 9:672
116. Johansen LD, Naumanen T, Knudsen A, Westerlund N, Gromova I et al (2008) IKAP localizes to membrane ruffles with filamin A and regulates actin cytoskeleton organization and cell migration. J Cell Sci 121:854-864
117. Yagi Y, Lim YM, Tsuda L, Nishida Y (2013) Fat facets induces polyubiquitination of Imd and inhibits the innate immune response in Drosophila. Genes Cells 18:934-945
118. den Hollander AI, Koenekoop RK, Mohamed MD, Arts HH, Boldt K et al (2007) Mutations in LCA5, encoding the ciliary protein lebercilin, cause Leber congenital amaurosis. Nat Genet 39:889-895
119. Bouwmeester T, Bauch A, Ruffner H, Angrand PO, Bergamini G et al (2004) A physical and functional map of the human TNF-alpha/NF-kappa B signal transduction pathway. Nat Cell Biol 6:97-105
120. Goncalves A, Burckstummer T, Dixit E, Scheicher R, Gorna MW et al (2011) Functional dissection of the TBK1 molecular network. PLoS One 6:e23971
121. Grasso D, Ropolo A, Lo Re A, Boggio V, Molejon MI et al (2011) Zymophagy, a novel selective autophagy pathway mediated by VMP1-USP9x-p62, prevents pancreatic cell death. J Biol Chem 286:8308-8324