USP7 Acts as a Molecular Rheostat to Promote WASH-Dependent Endosomal Protein Recycling and Is Mutated in a Human Neurodevelopmental Disorder

Molecular Cell

Volumn 59, Issue 6, 2015, Pages 956-969

  Hao, Yi Heng ^a   Fountain, Michael D ^b,c   Fon Tacer, Klementina ^a   Xia, Fan ^b   Bi, Weimin ^b   Kang, Sung Hae L ^b   Patel, Ankita ^b   Rosenfeld, Jill A ^b,k   Le Caignec, Cédric ^d   Isidor, Bertrand ^d   Krantz, Ian D ^e,f   Noon, Sarah E ^e   Pfotenhauer, Jean P ^g   Morgan, Thomas M ^g   Moran, Rocio ^h   Pedersen, Robert C ⁱ   Saenz, Margarita S ^j   Schaaf, Christian P ^b,c   Potts, Patrick Ryan ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

^c TEXAS CHILDREN S HOSPITAL   (United States)

^d NANTES UNIVERSITY HOSPITAL   (France)

^e CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

^f UNIVERSITY OF PENNSYLVANIA   (United States)

^g VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h LERNER RESEARCH INSTITUTE   (United States)

ⁱ TRIPLER ARMY MEDICAL CENTER   (United States)

^j CHILDREN S HOSPITAL COLORADO   (United States)

^k Signature Genomics   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; DEUBIQUITINASE; MEMBRANE PROTEIN; UNCLASSIFIED DRUG; USP7 PROTEIN; ACTIN BINDING PROTEIN; DNA BINDING PROTEIN; NUCLEAR PROTEIN; TRIM27 PROTEIN, HUMAN; UBIQUITIN THIOLESTERASE; USP7 PROTEIN, HUMAN; WASH PROTEIN, HUMAN;

ADOLESCENT; ARTICLE; AUTISM; CHILD; CLINICAL ARTICLE; CONTROLLED STUDY; ENDOSOMAL PROTEIN RECYCLING; FEMALE; HETEROZYGOTE; HUMAN; INTELLECTUAL IMPAIRMENT; LOSS OF FUNCTION MUTATION; MALE; NERVOUS SYSTEM DEVELOPMENT; NEUROLOGIC DISEASE; PROTEIN DEGRADATION; PROTEIN PROCESSING; SCHOOL CHILD; UBIQUITINATION; ENDOSOME; ENZYMOLOGY; FEEDBACK SYSTEM; GENE DELETION; GENETICS; HAPLOINSUFFICIENCY; HCT116 CELL LINE; HYPOTHALAMUS; METABOLISM; NERVE CELL; PHYSIOLOGY; PRESCHOOL CHILD; PROTEIN TRANSPORT;

ADOLESCENT; AUTISM SPECTRUM DISORDER; CHILD; CHILD, PRESCHOOL; DNA-BINDING PROTEINS; ENDOSOMES; FEEDBACK, PHYSIOLOGICAL; FEMALE; HAPLOINSUFFICIENCY; HCT116 CELLS; HUMANS; HYPOTHALAMUS; INTELLECTUAL DISABILITY; MALE; MICROFILAMENT PROTEINS; NEURONS; NUCLEAR PROTEINS; PROTEIN TRANSPORT; PROTEOLYSIS; SEQUENCE DELETION; UBIQUITIN THIOLESTERASE; UBIQUITINATION;

EID: 84941811672     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.07.033     Document Type: Article

References (40)

1. Bischof J.M., Stewart C.L., Wevrick R. Inactivation of the mouse Magel2 gene results in growth abnormalities similar to Prader-Willi syndrome. Hum. Mol. Genet. 2007, 16:2713-2719.
2. Boccaccio I., Glatt-Deeley H., Watrin F., Roëckel N., Lalande M., Muscatelli F. The human MAGEL2 gene and its mouse homologue are paternally expressed and mapped to the Prader-Willi region. Hum. Mol. Genet. 1999, 8:2497-2505.
3. Burd C., Cullen P.J. Retromer: a master conductor of endosome sorting. Cold Spring Harb. Perspect. Biol. 2014, 6:6.
4. Cassidy S.B., Schwartz S., Miller J.L., Driscoll D.J. Prader-Willi syndrome. Genet. Med. 2012, 14:10-26.
5. Cummins J.M., Vogelstein B. HAUSP is required for p53 destabilization. Cell Cycle 2004, 3:689-692.
6. Cummins J.M., Rago C., Kohli M., Kinzler K.W., Lengauer C., Vogelstein B. Tumour suppression: disruption of HAUSP gene stabilizes p53. Nature 2004, 428:486.
7. Derivery E., Sousa C., Gautier J.J., Lombard B., Loew D., Gautreau A. The Arp2/3 activator WASH controls the fission of endosomes through a large multiprotein complex. Dev. Cell 2009, 17:712-723.
8. Deshaies R.J., Joazeiro C.A. RING domain E3 ubiquitin ligases. Annu. Rev. Biochem. 2009, 78:399-434.
9. Doyle J.M., Gao J., Wang J., Yang M., Potts P.R. MAGE-RING protein complexes comprise a family of E3 ubiquitin ligases. Mol. Cell 2010, 39:963-974.
10. Faesen A.C., Dirac A.M., Shanmugham A., Ovaa H., Perrakis A., Sixma T.K. Mechanism of USP7/HAUSP activation by its C-terminal ubiquitin-like domain and allosteric regulation by GMP-synthetase. Mol. Cell 2011, 44:147-159.
11. Gomez T.S., Billadeau D.D. A FAM21-containing WASH complex regulates retromer-dependent sorting. Dev. Cell 2009, 17:699-711.
12. Hao Y.H., Doyle J.M., Ramanathan S., Gomez T.S., Jia D., Xu M., Chen Z.J., Billadeau D.D., Rosen M.K., Potts P.R. Regulation of WASH-dependent actin polymerization and protein trafficking by ubiquitination. Cell 2013, 152:1051-1064.
13. Jacobson L. Hypothalamic-pituitary-adrenocortical axis: neuropsychiatric aspects. Compr. Physiol. 2014, 4:715-738.
14. Jia D., Gomez T.S., Metlagel Z., Umetani J., Otwinowski Z., Rosen M.K., Billadeau D.D. WASH and WAVE actin regulators of the Wiskott-Aldrich syndrome protein (WASP) family are controlled by analogous structurally related complexes. Proc. Natl. Acad. Sci. USA 2010, 107:10442-10447.
15. Komander D., Rape M. The ubiquitin code. Annu. Rev. Biochem. 2012, 81:203-229.
16. Komander D., Clague M.J., Urbé S. Breaking the chains: structure and function of the deubiquitinases. Nat. Rev. Mol. Cell Biol. 2009, 10:550-563.
17. Kon N., Kobayashi Y., Li M., Brooks C.L., Ludwig T., Gu W. Inactivation of HAUSP in vivo modulates p53 function. Oncogene 2010, 29:1270-1279.
18. Kon N., Zhong J., Kobayashi Y., Li M., Szabolcs M., Ludwig T., Canoll P.D., Gu W. Roles of HAUSP-mediated p53 regulation in central nervous system development. Cell Death Differ. 2011, 18:1366-1375.
19. Kozlov S.V., Bogenpohl J.W., Howell M.P., Wevrick R., Panda S., Hogenesch J.B., Muglia L.J., Van Gelder R.N., Herzog E.D., Stewart C.L. The imprinted gene Magel2 regulates normal circadian output. Nat. Genet. 2007, 39:1266-1272.
20. Lee S., Kozlov S., Hernandez L., Chamberlain S.J., Brannan C.I., Stewart C.L., Wevrick R. Expression and imprinting of MAGEL2 suggest a role in Prader-willi syndrome and the homologous murine imprinting phenotype. Hum. Mol. Genet. 2000, 9:1813-1819.
21. Li M., Chen D., Shiloh A., Luo J., Nikolaev A.Y., Qin J., Gu W. Deubiquitination of p53 by HAUSP is an important pathway for p53 stabilization. Nature 2002, 416:648-653.
22. MacDonald E., Urbé S., Clague M.J. USP8 controls the trafficking and sorting of lysosomal enzymes. Traffic 2014, 15:879-888.
23. Mercer R.E., Wevrick R. Loss of magel2, a candidate gene for features of Prader-Willi syndrome, impairs reproductive function in mice. PLoS ONE 2009, 4:e4291.
24. Mercer R.E., Kwolek E.M., Bischof J.M., van Eede M., Henkelman R.M., Wevrick R. Regionally reduced brain volume, altered serotonin neurochemistry, and abnormal behavior in mice null for the circadian rhythm output gene Magel2. Am. J. Med. Genet. B. Neuropsychiatr. Genet. 2009, 150B:1085-1099.
25. Miller N.L., Wevrick R., Mellon P.L. Necdin, a Prader-Willi syndrome candidate gene, regulates gonadotropin-releasing hormone neurons during development. Hum. Mol. Genet. 2009, 18:248-260.
26. Nicholson B., Suresh Kumar K.G. The multifaceted roles of USP7: new therapeutic opportunities. Cell Biochem. Biophys. 2011, 60:61-68.
27. Potts P.R., Yu H. Human MMS21/NSE2 is a SUMO ligase required for DNA repair. Mol. Cell. Biol. 2005, 25:7021-7032.
28. Potts P.R., Yu H. The SMC5/6 complex maintains telomere length in ALT cancer cells through SUMOylation of telomere-binding proteins. Nat. Struct. Mol. Biol. 2007, 14:581-590.
29. Reyes-Turcu F.E., Ventii K.H., Wilkinson K.D. Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes. Annu. Rev. Biochem. 2009, 78:363-397.
30. Sanders S.J., Ercan-Sencicek A.G., Hus V., Luo R., Murtha M.T., Moreno-De-Luca D., Chu S.H., Moreau M.P., Gupta A.R., Thomson S.A., et al. Multiple recurrent de novo CNVs, including duplications of the 7q11.23 Williams syndrome region, are strongly associated with autism. Neuron 2011, 70:863-885.
31. Schaaf C.P., Gonzalez-Garay M.L., Xia F., Potocki L., Gripp K.W., Zhang B., Peters B.A., McElwain M.A., Drmanac R., Beaudet A.L., et al. Truncating mutations of MAGEL2 cause Prader-Willi phenotypes and autism. Nat. Genet. 2013, 45:1405-1408.
32. Schaefer J.B., Morgan D.O. Protein-linked ubiquitin chain structure restricts activity of deubiquitinating enzymes. J. Biol. Chem. 2011, 286:45186-45196.
33. Seaman M.N., Gautreau A., Billadeau D.D. Retromer-mediated endosomal protein sorting: all WASHed up!. Trends Cell Biol. 2013, 23:522-528.
34. Sheng Y., Saridakis V., Sarkari F., Duan S., Wu T., Arrowsmith C.H., Frappier L. Molecular recognition of p53 and MDM2 by USP7/HAUSP. Nat. Struct. Mol. Biol. 2006, 13:285-291.
35. St Pourcain B., Whitehouse A.J., Ang W.Q., Warrington N.M., Glessner J.T., Wang K., Timpson N.J., Evans D.M., Kemp J.P., Ring S.M., et al. Common variation contributes to the genetic architecture of social communication traits. Mol. Autism 2013, 4:34.
36. Tennese A.A., Wevrick R. Impaired hypothalamic regulation of endocrine function and delayed counterregulatory response to hypoglycemia in Magel2-null mice. Endocrinology 2011, 152:967-978.
37. Vilariño-Güell C., Wider C., Ross O.A., Dachsel J.C., Kachergus J.M., Lincoln S.J., Soto-Ortolaza A.I., Cobb S.A., Wilhoite G.J., Bacon J.A., et al. VPS35 mutations in Parkinson disease. Am. J. Hum. Genet. 2011, 89:162-167.
38. Watson J.A., Bhattacharyya B.J., Vaden J.H., Wilson J.A., Icyuz M., Howard A.D., Phillips E., DeSilva T.M., Siegal G.P., Bean A.J., et al. Motor and Sensory Deficits in the teetering Mice Result from Mutation of the ESCRT Component HGS. PLoS Genet. 2015, 11:e1005290.
39. Wetsel W.C., Mellon P.L., Weiner R.I., Negro-Vilar A. Metabolism of pro-luteinizing hormone-releasing hormone in immortalized hypothalamic neurons. Endocrinology 1991, 129:1584-1595.
40. Zaman M.M., Nomura T., Takagi T., Okamura T., Jin W., Shinagawa T., Tanaka Y., Ishii S. Ubiquitination-deubiquitination by the TRIM27-USP7 complex regulates tumor necrosis factor alpha-induced apoptosis. Mol. Cell. Biol. 2013, 33:4971-4984.