RBR E3-ligases at work

EMBO Reports

Volumn 15, Issue 2, 2014, Pages 142-154

  Smit, Judith J ^a   Sixma, Titia K ^a  

^a NETHERLANDS CANCER INSTITUTE   (Netherlands)

Author keywords

autoinhibition; E3 ligase; mechanism; RBR; TRIAD; ubiquitination

Indexed keywords

CYSTEINE; GROWTH FACTOR INDEPENDENCE 1 PROTEIN; HEME OXIDIZED IRP2 UBIQUITIN LIGASE 1; HOMOLOGOUS TO THE E 6 AP CARBOXY TERMINUS PROTEIN; HUMAN HOMOLOGUE OF DROSOPHILA ARIADNE PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN ESSENTIAL MODULATOR PROTEIN; NPL 4 ZINC FINGER PROTEIN; PARKIN; PROTEIN; PROTEIN TRIAD; RING IBR RING LIGASE; UBIQUITIN; UBIQUITIN CONJUGATING ENZYME E2; UBIQUITIN PROTEIN LIGASE; UBIQUITIN PROTEIN LIGASE E3; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; CELL FUNCTION; CONJUGATION; ENZYME ACTIVITY; ENZYME REGULATION; ENZYME STRUCTURE; GENE; HUMAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; REALLY INTERESTING NEW GENE; REVIEW; RING FINGER MOTIF;

AMINO ACID SEQUENCE; ANIMALS; CATALYTIC DOMAIN; HUMANS; MOLECULAR SEQUENCE DATA; RING FINGER DOMAINS; UBIQUITIN-PROTEIN LIGASES;

EID: 84898614605     PISSN: 1469221X     EISSN: 14693178     Source Type: Journal    
DOI: 10.1002/embr.201338166     Document Type: Review

References (124)

1. Wenzel DM, Lissounov A, Brzovic PS, Klevit RE, (2011) UBCH7 reactivity profile reveals parkin and HHARI to be RING/HECT hybrids. Nature 474: 105-108
2. Morett E, Bork P, (1999) A novel transactivation domain in parkin. Trends Biochem Sci 24: 229-231 (Pubitemid 29317288)
3. van der Reijden BA, Erpelinck-Verschueren CA, Lowenberg B, Jansen JH, (1999) TRIADs: a new class of proteins with a novel cysteine-rich signature. Protein Sci 8: 1557-1561 (Pubitemid 29328239)
4. Marin I, Ferrus A, (2002) Comparative genomics of the RBR family, including the Parkinson's disease-related gene parkin and the genes of the ariadne subfamily. Mol Biol Evol 19: 2039-2050 (Pubitemid 35440440)
5. Marin I, Lucas JI, Gradilla AC, Ferrus A, (2004) Parkin and relatives: the RBR family of ubiquitin ligases. Physiol Genomics 17: 253-263 (Pubitemid 38924170)
6. Smit JJ, Monteferrario D, Noordermeer SM, van Dijk WJ, van der Reijden BA, Sixma TK, (2012) The E3 ligase HOIP specifies linear ubiquitin chain assembly through its RING-IBR-RING domain and the unique LDD extension. EMBO J 31: 3833-3844
7. Stieglitz B, Morris-Davies AC, Koliopoulos MG, Christodoulou E, Rittinger K, (2012) LUBAC synthesizes linear ubiquitin chains via a thioester intermediate. EMBO Rep 13: 840-846
8. Chaugule VK, Burchell L, Barber KR, Sidhu A, Leslie SJ, Shaw GS, Walden H, (2011) Autoregulation of Parkin activity through its ubiquitin-like domain. EMBO J 30: 2853-2867
9. Riley BE, Lougheed JC, Callaway K, Velasquez M, Brecht E, Nguyen L, Shaler T, Walker D, Yang Y, Regnstrom K, Diep L, Zhang Z, Chiou S, Bova M, Artis DR, Yao N, Baker J, Yednock T, Johnston JA, (2013) Structure and function of Parkin E3 ubiquitin ligase reveals aspects of RING and HECT ligases. Nat Commun 4: 1982
10. Trempe JF, Sauve V, Grenier K, Seirafi M, Tang MY, Menade M, Al-Abdul-Wahid S, Krett J, Wong K, Kozlov G, Nagar B, Fon EA, Gehring K, (2013) Structure of parkin reveals mechanisms for ubiquitin ligase activation. Science 340: 1451-1455
11. Wauer T, Komander D, (2013) Structure of the human Parkin ligase domain in an autoinhibited state. EMBO J 32: 2099-2112
12. Eisenhaber B, Chumak N, Eisenhaber F, Hauser MT, (2007) The ring between ring fingers (RBR) protein family. Genome Biol 8: 209
13. Belgnaoui SM, Paz S, Samuel S, Goulet ML, Sun Q, Kikkert M, Iwai K, Dikic I, Hiscott J, Lin R, (2012) Linear ubiquitination of NEMO negatively regulates the interferon antiviral response through disruption of the MAVS-TRAF3 complex. Cell Host Microbe 12: 211-222
14. Seymour RE, Hasham MG, Cox GA, Shultz LD, Hogenesch H, Roopenian DC, Sundberg JP, (2007) Spontaneous mutations in the mouse Sharpin gene result in multiorgan inflammation, immune system dysregulation and dermatitis. Genes Immun 8: 416-421 (Pubitemid 47163104)
15. Boisson B, Laplantine E, Prando C, Giliani S, Israelsson E, Xu Z, Abhyankar A, Israël L, Trevejo-Nunez G, Bogunovic D, Cepika AM, MacDuff D, Chrabieh M, Hubeau M, Bajolle F, Debré M, Mazzolari E, Vairo D, Agou F, Virgin HW, et al, (2012) Immunodeficiency, autoinflammation and amylopectinosis in humans with inherited HOIL-1 and LUBAC deficiency. Nat Immunol 13: 1178-1186
16. Darios F, Corti O, Lucking CB, Hampe C, Muriel MP, Abbas N, Gu WJ, Hirsch EC, Rooney T, Ruberg M, Brice A, (2003) Parkin prevents mitochondrial swelling and cytochrome c release in mitochondria-dependent cell death. Hum Mol Genet 12: 517-526 (Pubitemid 36305590)
17. Kitada T, Asakawa S, Hattori N, Matsumine H, Yamamura Y, Minoshima S, Yokochi M, Mizuno Y, Shimizu N, (1998) Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism. Nature 392: 605-608 (Pubitemid 28207717)
18. Matsumine H, Saito M, Shimoda-Matsubayashi S, Tanaka H, Ishikawa A, Nakagawa-Hattori Y, Yokochi M, Kobayashi T, Igarashi S, Takano H, Sanpei K, Koike R, Mori H, Kondo T, Mizutani Y, Schäffer AA, Yamamura Y, Nakamura S, Kuzuhara S, Tsuji S, et al, (1997) Localization of a gene for an autosomal recessive form of juvenile Parkinsonism to chromosome 6q25.2-27. Am J Hum Genet 60: 588-596 (Pubitemid 27097607)
19. Poulogiannis G, McIntyre RE, Dimitriadi M, Apps JR, Wilson CH, Ichimura K, Luo F, Cantley LC, Wyllie AH, Adams DJ, Arends MJ, (2010) PARK2 deletions occur frequently in sporadic colorectal cancer and accelerate adenoma development in Apc mutant mice. Proc Natl Acad Sci USA 107: 15145-15150
20. Veeriah S, Morris L, Solit D, Chan TA, (2010) The familial Parkinson disease gene PARK2 is a multisite tumor suppressor on chromosome 6q25.2-27 that regulates cyclin E. Cell Cycle 9: 1451-1452
21. Narendra D, Tanaka A, Suen DF, Youle RJ, (2008) Parkin is recruited selectively to impaired mitochondria and promotes their autophagy. J Cell Biol 183: 795-803
22. Lazarou M, Narendra DP, Jin SM, Tekle E, Banerjee S, Youle RJ, (2013) PINK1 drives Parkin self-association and HECT-like E3 activity upstream of mitochondrial binding. J Cell Biol 200: 163-172
23. Shimura H, Schlossmacher MG, Hattori N, Frosch MP, Trockenbacher A, Schneider R, Mizuno Y, Kosik KS, Selkoe DJ, (2001) Ubiquitination of a new form of alpha-synuclein by parkin from human brain: implications for Parkinson's disease. Science 293: 263-269 (Pubitemid 32694735)
24. Zhang Y, Gao J, Chung KK, Huang H, Dawson VL, Dawson TM, (2000) Parkin functions as an E2-dependent ubiquitin- protein ligase and promotes the degradation of the synaptic vesicle-associated protein, CDCrel-1. Proc Natl Acad Sci USA 97: 13354-13359
25. Imai Y, Soda M, Inoue H, Hattori N, Mizuno Y, Takahashi R, (2001) An unfolded putative transmembrane polypeptide, which can lead to endoplasmic reticulum stress, is a substrate of Parkin. Cell 105: 891-902 (Pubitemid 32635090)
26. Olzmann JA, Li L, Chudaev MV, Chen J, Perez FA, Palmiter RD, Chin LS, (2007) Parkin-mediated K63-linked polyubiquitination targets misfolded DJ-1 to aggresomes via binding to HDAC6. J Cell Biol 178: 1025-1038 (Pubitemid 47443324)
27. Jenner P, Olanow CW, (1998) Understanding cell death in Parkinson's disease. Ann Neurol 44: S72-S84 (Pubitemid 28423832)
28. Burchell VS, Nelson DE, Sanchez-Martinez A, Delgado-Camprubi M, Ivatt RM, Pogson JH, Randle SJ, Wray S, Lewis PA, Houlden H, Abramov AY, Hardy J, Wood NW, Whitworth AJ, Laman H, Plun-Favreau H, (2013) The Parkinson's disease-linked proteins Fbxo7 and Parkin interact to mediate mitophagy. Nat Neurosci 16: 1257-1265
29. Manzanillo PS, Ayres JS, Watson RO, Collins AC, Souza G, Rae CS, Schneider DS, Nakamura K, Shiloh MU, Cox JS, (2013) The ubiquitin ligase parkin mediates resistance to intracellular pathogens. Nature 501: 512-516
30. Gegg ME, Cooper JM, Chau KY, Rojo M, Schapira AH, Taanman JW, (2010) Mitofusin 1 and mitofusin 2 are ubiquitinated in a PINK1/parkin-dependent manner upon induction of mitophagy. Hum Mol Genet 19: 4861-4870
31. Okatsu K, Iemura S, Koyano F, Go E, Kimura M, Natsume T, Tanaka K, Matsuda N, (2012) Mitochondrial hexokinase HKI is a novel substrate of the Parkin ubiquitin ligase. Biochem Biophys Res Commun 428: 197-202
32. Ziviani E, Tao RN, Whitworth AJ, (2010) Drosophila parkin requires PINK1 for mitochondrial translocation and ubiquitinates mitofusin. Proc Natl Acad Sci USA 107: 5018-5023
33. Corti O, Hampe C, Koutnikova H, Darios F, Jacquier S, Prigent A, Robinson JC, Pradier L, Ruberg M, Mirande M, Hirsch E, Rooney T, Fournier A, Brice A, (2003) The p38 subunit of the aminoacyl-tRNA synthetase complex is a Parkin substrate: linking protein biosynthesis and neurodegeneration. Hum Mol Genet 12: 1427-1437 (Pubitemid 36758455)
34. Um JW, Chung KC, (2006) Functional modulation of parkin through physical interaction with SUMO-1. J Neurosci Res 84: 1543-1554 (Pubitemid 44683147)
35. Okui M, Yamaki A, Takayanagi A, Kudoh J, Shimizu N, Shimizu Y, (2005) Transcription factor single-minded 2 (SIM2) is ubiquitinated by the RING-IBR-RING-type E3 ubiquitin ligases. Exp Cell Res 309: 220-228 (Pubitemid 41191236)
36. Chen D, Gao F, Li B, Wang H, Xu Y, Zhu C, Wang G, (2010) Parkin mono-ubiquitinates Bcl-2 and regulates autophagy. J Biol Chem 285: 38214-38223
37. Sarraf SA, Raman M, Guarani-Pereira V, Sowa ME, Huttlin EL, Gygi SP, Harper JW, (2013) Landscape of the PARKIN-dependent ubiquitylome in response to mitochondrial depolarization. Nature 496: 372-376
38. Ardley HC, Tan NG, Rose SA, Markham AF, Robinson PA, (2001) Features of the parkin/ariadne-like ubiquitin ligase, HHARI, that regulate its interaction with the ubiquitin-conjugating enzyme, Ubch7. J Biol Chem 276: 19640-19647
39. Parelkar SS, Cadena JG, Kim C, Wang Z, Sugal R, Bentley B, Moral L, Ardley HC, Schwartz LM, (2012) The Parkin-like human homolog of Drosophila ariadne-1 (HHARI) can induce aggresome formation in mammalian cells and is immunologically detectable in Lewy bodies. J Mol Neurosci 46: 109-121
40. Tan NG, Ardley HC, Scott GB, Rose SA, Markham AF, Robinson PA, (2003) Human homologue of ariadne promotes the ubiquitylation of translation initiation factor 4E homologous protein, 4EHP. FEBS Lett 554: 501-504 (Pubitemid 37412539)
41. Elmehdawi F, Wheway G, Szymanska K, Adams M, High AS, Johnson CA, Robinson PA, (2013) Human Homolog of Drosophila Ariadne (HHARI) is a marker of cellular proliferation associated with nuclear bodies. Exp Cell Res 319: 161-172
42. Kelsall IR, Duda DM, Olszewski JL, Hofmann K, Knebel A, Langevin F, Wood N, Wightman M, Schulman BA, Alpi AF, (2013) TRIAD1 and HHARI bind to and are activated by distinct neddylated Cullin-RING ligase complexes. EMBO J 32: 2848-2860
43. Lin AE, Ebert G, Ow Y, Preston SP, Toe JG, Cooney JP, Scott HW, Sasaki M, Saibil SD, Dissanayake D, Kim RH, Wakeham A, You-Ten A, Shahinian A, Duncan G, Silvester J, Ohashi PS, Mak TW, Pellegrini M, (2013) ARIH2 is essential for embryogenesis, and its hematopoietic deficiency causes lethal activation of the immune system. Nat Immunol 14: 27-33
44. Hassink G, Slotman J, Oorschot V, Van Der Reijden BA, Monteferrario D, Noordermeer SM, Van Kerkhof P, Klumperman J, Strous GJ, (2012) Identification of the ubiquitin ligase Triad1 as a regulator of endosomal transport. Biol Open 1: 607-614
45. Wang H, Bei L, Shah CA, Horvath E, Eklund EA, (2011) HoxA10 influences protein ubiquitination by activating transcription of ARIH2, the gene encoding Triad1. J Biol Chem 286: 16832-16845
46. Bae S, Jung JH, Kim K, An IS, Kim SY, Lee JH, Park IC, Jin YW, Lee SJ, An S, (2012) TRIAD1 inhibits MDM2-mediated p53 ubiquitination and degradation. FEBS Lett 586: 3057-3063
47. Marteijn JA, van der Meer LT, van Emst L, van Reijmersdal S, Wissink W, de Witte T, Jansen JH, Van der Reijden BA, (2007) Gfi1 ubiquitination and proteasomal degradation is inhibited by the ubiquitin ligase Triad1. Blood 110: 3128-3135 (Pubitemid 350106303)
48. Marteijn JA, van Emst L, Erpelinck-Verschueren CA, Nikoloski G, Menke A, de Witte T, Lowenberg B, Jansen JH, van der Reijden BA, (2005) The E3 ubiquitin-protein ligase Triad1 inhibits clonogenic growth of primary myeloid progenitor cells. Blood 106: 4114-4123 (Pubitemid 41775916)
49. Wang W, Yoder JH, (2012) Hox-mediated regulation of doublesex sculpts sex-specific abdomen morphology in Drosophila. Dev Dyn 241: 1076-1090
50. Marteijn JA, van der Meer LT, Smit JJ, Noordermeer SM, Wissink W, Jansen P, Swarts HG, Hibbert RG, de Witte T, Sixma TK, Jansen JH, van der Reijden BA, (2009) The ubiquitin ligase Triad1 inhibits myelopoiesis through UbcH7 and Ubc13 interacting domains. Leukemia 23: 1480-1489
51. Kawagoe H, Humphries RK, Blair A, Sutherland HJ, Hogge DE, (1999) Expression of HOX genes, HOX cofactors, and MLL in phenotypically and functionally defined subpopulations of leukemic and normal human hematopoietic cells. Leukemia 13: 687-698 (Pubitemid 29243618)
52. Camos M, Esteve J, Jares P, Colomer D, Rozman M, Villamor N, Costa D, Carrio A, Nomdedeu J, Montserrat E, Campo E, (2006) Gene expression profiling of acute myeloid leukemia with translocation t(8;16)(p11;p13) and MYST3-CREBBP rearrangement reveals a distinctive signature with a specific pattern of HOX gene expression. Cancer Res 66: 6947-6954 (Pubitemid 44197669)
53. Sauvageau G, Lansdorp PM, Eaves CJ, Hogge DE, Dragowska WH, Reid DS, Largman C, Lawrence HJ, Humphries RK, (1994) Differential expression of homeobox genes in functionally distinct CD34+ subpopulations of human bone marrow cells. Proc Natl Acad Sci USA 91: 12223-12227 (Pubitemid 24368637)
54. Armstrong SA, Staunton JE, Silverman LB, Pieters R, den Boer ML, Minden MD, Sallan SE, Lander ES, Golub TR, Korsmeyer SJ, (2002) MLL translocations specify a distinct gene expression profile that distinguishes a unique leukemia. Nat Genet 30: 41-47
55. Gerlach B, Cordier SM, Schmukle AC, Emmerich CH, Rieser E, Haas TL, Webb AI, Rickard JA, Anderton H, Wong WW, Nachbur U, Gangoda L, Warnken U, Purcell AW, Silke J, Walczak H, (2011) Linear ubiquitination prevents inflammation and regulates immune signalling. Nature 471: 591-596
56. Ikeda F, Deribe YL, Skånland SS, Stieglitz B, Grabbe C, Franz-Wachtel M, van Wijk SJ, Goswami P, Nagy V, Terzic J, Tokunaga F, Androulidaki A, Nakagawa T, Pasparakis M, Iwai K, Sundberg JP, Schaefer L, Rittinger K, Macek B, Dikic I, (2011) SHARPIN forms a linear ubiquitin ligase complex regulating NF-kappaB activity and apoptosis. Nature 471: 637-641
57. Kirisako T, Kamei K, Murata S, Kato M, Fukumoto H, Kanie M, Sano S, Tokunaga F, Tanaka K, Iwai K, (2006) A ubiquitin ligase complex assembles linear polyubiquitin chains. EMBO J 25: 4877-4887 (Pubitemid 44607032)
58. Tokunaga F, Sakata S, Saeki Y, Satomi Y, Kirisako T, Kamei K, Nakagawa T, Kato M, Murata S, Yamaoka S, Yamamoto M, Akira S, Takao T, Tanaka K, Iwai K, (2009) Involvement of linear polyubiquitylation of NEMO in NF-kappaB activation. Nat Cell Biol 11: 123-132
59. Tokunaga F, Nakagawa T, Nakahara M, Saeki Y, Taniguchi M, Sakata S, Tanaka K, Nakano H, Iwai K, (2011) SHARPIN is a component of the NF-kappaB-activating linear ubiquitin chain assembly complex. Nature 471: 633-636
60. Hostager BS, Fox DK, Whitten D, Wilkerson CG, Eipper BA, Francone VP, Rothman PB, Colgan JD, (2010) HOIL-1L interacting protein (HOIP) as an NF-kappaB regulating component of the CD40 signaling complex. PLoS ONE 5: e11380
61. Smit JJ, van Dijk WJ, El Atmioui D, Merkx R, Ovaa H, Sixma TK, (2013) Target Specificity of the E3 Ligase LUBAC for Ubiquitin and NEMO Relies on Different Minimal Requirements. J Biol Chem 288: 31728-31737
62. Haas TL, Emmerich CH, Gerlach B, Schmukle AC, Cordier SM, Rieser E, Feltham R, Vince J, Warnken U, Wenger T, Koschny R, Komander D, Silke J, Walczak H, (2009) Recruitment of the linear ubiquitin chain assembly complex stabilizes the TNF-R1 signaling complex and is required for TNF-mediated gene induction. Mol Cell 36: 831-844
63. Emmerich CH, Ordureau A, Strickson S, Arthur JS, Pedrioli PG, Komander D, Cohen P, (2013) Activation of the canonical IKK complex by K63/M1-linked hybrid ubiquitin chains. Proc Natl Acad Sci USA 110: 15247-15252
64. Fiil BK, Damgaard RB, Wagner SA, Keusekotten K, Fritsch M, Bekker-Jensen S, Mailand N, Choudhary C, Komander D, Gyrd-Hansen M, (2013) OTULIN restricts Met1-linked ubiquitination to control innate immune signaling. Mol Cell 50: 818-830
65. Muller-Rischart AK, et al, (2013) The E3 ligase parkin maintains mitochondrial integrity by increasing linear ubiquitination of NEMO. Mol Cell 49: 908-921
66. Müller-Rischart AK, Pilsl A, Beaudette P, Patra M, Hadian K, Funke M, Peis R, Deinlein A, Schweimer C, Kuhn PH, Lichtenthaler SF, Motori E, Hrelia S, Wurst W, Trümbach D, Langer T, Krappmann D, Dittmar G, Tatzelt J, Winklhofer KF, (2009) Specific recognition of linear ubiquitin chains by NEMO is important for NF-kappaB activation. Cell 136: 1098-1109
67. Sato Y, Fujita H, Yoshikawa A, Yamashita M, Yamagata A, Kaiser SE, Iwai K, Fukai S, (2011) Specific recognition of linear ubiquitin chains by the Npl4 zinc finger (NZF) domain of the HOIL-1L subunit of the linear ubiquitin chain assembly complex. Proc Natl Acad Sci USA 108: 20520-20525
68. Wagner S, Carpentier I, Rogov V, Kreike M, Ikeda F, Lohr F, Wu CJ, Ashwell JD, Dotsch V, Dikic I, Beyaert R, (2008) Ubiquitin binding mediates the NF-kappaB inhibitory potential of ABIN proteins. Oncogene 27: 3739-3745 (Pubitemid 351912974)
69. Kensche T, Tokunaga F, Ikeda F, Goto E, Iwai K, Dikic I, (2012) Analysis of nuclear factor-kappaB (NF-kappaB) essential modulator (NEMO) binding to linear and lysine-linked ubiquitin chains and its role in the activation of NF-kappaB. J Biol Chem 287: 23626-23634
70. Verhelst K, Carpentier I, Kreike M, Meloni L, Verstrepen L, Kensche T, Dikic I, Beyaert R, (2012) A20 inhibits LUBAC-mediated NF-kappaB activation by binding linear polyubiquitin chains via its zinc finger 7. EMBO J 31: 3845-3855
71. Keusekotten K, Elliott PR, Glockner L, Fiil BK, Damgaard RB, Kulathu Y, Wauer T, Hospenthal MK, Gyrd-Hansen M, Krappmann D, Hofmann K, Komander D, (2013) OTULIN antagonizes LUBAC signaling by specifically hydrolyzing Met1-linked polyubiquitin. Cell 153: 1312-1326
72. Rivkin E, Almeida SM, Ceccarelli DF, Juang YC, MacLean TA, Srikumar T, Huang H, Dunham WH, Fukumura R, Xie G, Gondo Y, Raught B, Gingras AC, Sicheri F, Cordes SP, (2013) The linear ubiquitin-specific deubiquitinase gumby regulates angiogenesis. Nature 498: 318-324
73. Zinngrebe J, Montinaro A, Peltzer N, Walczak H, (2014) Ubiquitin in the immune system. EMBO Rep
74. Chew KC, Matsuda N, Saisho K, Lim GG, Chai C, Tan HM, Tanaka K, Lim KL, (2011) Parkin mediates apparent E2-independent monoubiquitination in vitro and contains an intrinsic activity that catalyzes polyubiquitination. PLoS ONE 6: e19720
75. Petroski MD, Deshaies RJ, (2005) Mechanism of lysine 48-linked ubiquitin-chain synthesis by the cullin-RING ubiquitin-ligase complex SCF-Cdc34. Cell 123: 1107-1120 (Pubitemid 41785424)
76. Seol JH, Feldman RM, Zachariae W, Shevchenko A, Correll CC, Lyapina S, Chi Y, Galova M, Claypool J, Sandmeyer S, Nasmyth K, Deshaies RJ, (1999) Cdc53/cullin and the essential Hrt1 RING-H2 subunit of SCF define a ubiquitin ligase module that activates the E2 enzyme Cdc34. Genes Dev 13: 1614-1626 (Pubitemid 29297928)
77. Duda DM, Olszewski JL, Schuermann JP, Kurinov I, Miller DJ, Nourse A, Alpi AF, Schulman BA, (2013) Structure of HHARI, a RING-IBR-RING ubiquitin ligase: autoinhibition of an Ariadne-family E3 and insights into ligation mechanism. Structure 21: 1030-1041
78. Plechanovova A, Jaffray EG, Tatham MH, Naismith JH, Hay RT, (2012) Structure of a RING E3 ligase and ubiquitin-loaded E2 primed for catalysis. Nature 489: 115-120
79. Pruneda JN, Littlefield PJ, Soss SE, Nordquist KA, Chazin WJ, Brzovic PS, Klevit RE, (2012) Structure of an E3:E2~Ub complex reveals an allosteric mechanism shared among RING/U-box ligases. Mol Cell 47: 933-942
80. Dou H, Buetow L, Hock A, Sibbet GJ, Vousden KH, Huang DT, (2012) Structural basis for autoinhibition and phosphorylation-dependent activation of c-Cbl. Nat Struct Mol Biol 19: 184-192
81. Spratt DE, Martinez-Torres RJ, Noh YJ, Mercier P, Manczyk N, Barber KR, Aguirre JD, Burchell L, Purkiss A, Walden H, Shaw GS, (2013) A molecular explanation for the recessive nature of parkin-linked Parkinson's disease. Nat Commun 4: 1983
82. Stieglitz B, Rana RR, Koliopoulos MG, Morris-Davies AC, Schaeffer V, Christodoulou E, Howell S, Brown NR, Dikic I, Rittinger K, (2013) Structural basis for ligase-specific conjugation of linear ubiquitin chains by HOIP. Nature 503: 422-426
83. Frye JJ, Brown NG, Petzold G, Watson ER, Grace CR, Nourse A, Jarvis MA, Kriwacki RW, Peters JM, Stark H, Schulman BA, (2013) Electron microscopy structure of human APC/C(CDH1)-EMI1 reveals multimodal mechanism of E3 ligase shutdown. Nat Struct Mol Biol 20: 827-835
84. Fallon L, Belanger CM, Corera AT, Kontogiannea M, Regan-Klapisz E, Moreau F, Voortman J, Haber M, Rouleau G, Thorarinsdottir T, Brice A, van Bergen En Henegouwen PM, Fon EA, (2006) A regulated interaction with the UIM protein Eps15 implicates parkin in EGF receptor trafficking and PI(3)K-Akt signalling. Nat Cell Biol 8: 834-842 (Pubitemid 44151586)
85. Tsai YC, Fishman PS, Thakor NV, Oyler GA, (2003) Parkin facilitates the elimination of expanded polyglutamine proteins and leads to preservation of proteasome function. J Biol Chem 278: 22044-22055 (Pubitemid 36792614)
86. Um JW, Han KA, Im E, Oh Y, Lee K, Chung KC, (2012) Neddylation positively regulates the ubiquitin E3 ligase activity of parkin. J Neurosci Res 90: 1030-1042
87. Kondapalli C, Kazlauskaite A, Zhang N, Woodroof HI, Campbell DG, Gourlay R, Burchell L, Walden H, Macartney TJ, Deak M, Knebel A, Alessi DR, Muqit MM, (2012) PINK1 is activated by mitochondrial membrane potential depolarization and stimulates Parkin E3 ligase activity by phosphorylating Serine 65. Open Biol 2: 120080
88. Shiba-Fukushima K, Imai Y, Yoshida S, Ishihama Y, Kanao T, Sato S, Hattori N, (2012) PINK1-mediated phosphorylation of the Parkin ubiquitin-like domain primes mitochondrial translocation of Parkin and regulates mitophagy. Sci Rep 2: 1002
89. Sha D, Chin LS, Li L, (2010) Phosphorylation of parkin by Parkinson disease-linked kinase PINK1 activates parkin E3 ligase function and NF-kappaB signaling. Hum Mol Genet 19: 352-363
90. Imam SZ, Zhou Q, Yamamoto A, Valente AJ, Ali SF, Bains M, Roberts JL, Kahle PJ, Clark RA, Li S, (2011) Novel regulation of parkin function through c-Abl-mediated tyrosine phosphorylation: implications for Parkinson's disease. J Neurosci 31: 157-163
91. Chung KK, Thomas B, Li X, Pletnikova O, Troncoso JC, Marsh L, Dawson VL, Dawson TM, (2004) S-nitrosylation of parkin regulates ubiquitination and compromises parkin's protective function. Science 304: 1328-1331 (Pubitemid 38697430)
92. Ozawa K, Komatsubara AT, Nishimura Y, Sawada T, Kawafune H, Tsumoto H, Tsuji Y, Zhao J, Kyotani Y, Tanaka T, Takahashi R, Yoshizumi M, (2013) S-nitrosylation regulates mitochondrial quality control via activation of parkin. Sci Rep 3: 2202
93. Ischiropoulos H, (2003) Oxidative modifications of alpha-synuclein. Ann N Y Acad Sci 991: 93-100
94. Haddad DM, Vilain S, Vos M, Esposito G, Matta S, Kalscheuer VM, Craessaerts K, Leyssen M, Nascimento RM, Vianna-Morgante AM, De Strooper B, Van Esch H, Morais VA, Verstreken P, (2013) Mutations in the intellectual disability gene Ube2a cause neuronal dysfunction and impair parkin-dependent mitophagy. Mol Cell 50: 831-843
95. Rankin CA, Joazeiro CA, Floor E, Hunter T, (2001) E3 ubiquitin-protein ligase activity of Parkin is dependent on cooperative interaction of RING finger (TRIAD) elements. J Biomed Sci 8: 421-429 (Pubitemid 32830592)
96. Capili AD, Edghill EL, Wu K, Borden KL, (2004) Structure of the C-terminal RING finger from a RING-IBR-RING/TRIAD motif reveals a novel zinc-binding domain distinct from a RING. J Mol Biol 340: 1117-1129 (Pubitemid 38968705)
97. Hampe C, Ardila-Osorio H, Fournier M, Brice A, Corti O, (2006) Biochemical analysis of Parkinson's disease-causing variants of Parkin, an E3 ubiquitin-protein ligase with monoubiquitylation capacity. Hum Mol Genet 15: 2059-2075 (Pubitemid 43923396)
98. Matsuda N, Kitami T, Suzuki T, Mizuno Y, Hattori N, Tanaka K, (2006) Diverse effects of pathogenic mutations of Parkin that catalyze multiple monoubiquitylation in vitro. J Biol Chem 281: 3204-3209 (Pubitemid 43845931)
99. Staropoli JF, McDermott C, Martinat C, Schulman B, Demireva E, Abeliovich A, (2003) Parkin is a component of an SCF-like ubiquitin ligase complex and protects postmitotic neurons from kainate excitotoxicity. Neuron 37: 735-749 (Pubitemid 36288547)
100. Doss-Pepe EW, Chen L, Madura K, (2005) Alpha-synuclein and parkin contribute to the assembly of ubiquitin lysine 63-linked multiubiquitin chains. J Biol Chem 280: 16619-16624 (Pubitemid 41389118)
101. Lim KL, Chew KC, Tan JM, Wang C, Chung KK, Zhang Y, Tanaka Y, Smith W, Engelender S, Ross CA, Dawson VL, Dawson TM, (2005) Parkin mediates nonclassical, proteasomal-independent ubiquitination of synphilin-1: implications for Lewy body formation. J Neurosci 25: 2002-2009 (Pubitemid 40289405)
102. Moore DJ, West AB, Dikeman DA, Dawson VL, Dawson TM, (2008) Parkin mediates the degradation-independent ubiquitination of Hsp70. J Neurochem 105: 1806-1819 (Pubitemid 351678490)
103. Moynihan TP, Ardley HC, Nuber U, Rose SA, Jones PF, Markham AF, Scheffner M, Robinson PA, (1999) The ubiquitin-conjugating enzymes UbcH7 and UbcH8 interact with RING finger/IBR motif-containing domains of HHARI and H7-AP1. J Biol Chem 274: 30963-30968
104. Li W, Tu D, Li L, Wollert T, Ghirlando R, Brunger AT, Ye Y, (2009) Mechanistic insights into active site-associated polyubiquitination by the ubiquitin-conjugating enzyme Ube2g2. Proc Natl Acad Sci USA 106: 3722-3727
105. Inn KS, Gack MU, Tokunaga F, Shi M, Wong LY, Iwai K, Jung JU, (2011) Linear ubiquitin assembly complex negatively regulates RIG-I- and TRIM25-mediated type I interferon induction. Mol Cell 41: 354-365
106. Aguilera M, Oliveros M, Martinez-Padron M, Barbas JA, Ferrus A, (2000) Ariadne-1: a vital Drosophila gene is required in development and defines a new conserved family of ring-finger proteins. Genetics 155: 1231-1244 (Pubitemid 30463433)
107. Stelzl U, Worm U, Lalowski M, Haenig C, Brembeck FH, Goehler H, Stroedicke M, Zenkner M, Schoenherr A, Koeppen S, Timm J, Mintzlaff S, Abraham C, Bock N, Kietzmann S, Goedde A, Toksöz E, Droege A, Krobitsch S, Korn B, (2005) A human protein-protein interaction network: a resource for annotating the proteome. Cell 122: 957-968 (Pubitemid 41345212)
108. Markson G, Kiel C, Hyde R, Brown S, Charalabous P, Bremm A, Semple J, Woodsmith J, Duley S, Salehi-Ashtiani K, Vidal M, Komander D, Serrano L, Lehner P, Sanderson CM, (2009) Analysis of the human E2 ubiquitin conjugating enzyme protein interaction network. Genome Res 19: 1905-1911
109. Nikolaev AY, Li M, Puskas N, Qin J, Gu W, (2003) Parc: a cytoplasmic anchor for p53. Cell 112: 29-40 (Pubitemid 36106416)
110. Shimura H, Hattori N, Kubo S, Mizuno Y, Asakawa S, Minoshima S, Shimizu N, Iwai K, Chiba T, Tanaka K, Suzuki T, (2000) Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase. Nat Genet 25: 302-305 (Pubitemid 30437317)
111. Martinez-Noel G, Muller U, Harbers K, (2001) Identification of molecular determinants required for interaction of ubiquitin-conjugating enzymes and RING finger proteins. Eur J Biochem 268: 5912-5919 (Pubitemid 33079327)
112. Ng CC, Arakawa H, Fukuda S, Kondoh H, Nakamura Y, (2003) p53RFP, a p53-inducible RING-finger protein, regulates the stability of p21WAF1. Oncogene 22: 4449-4458 (Pubitemid 36897976)
113. Huang J, Xu LG, Liu T, Zhai Z, Shu HB, (2006) The p53-inducible E3 ubiquitin ligase p53RFP induces p53-dependent apoptosis. FEBS Lett 580: 940-947 (Pubitemid 43152318)
114. van Wijk SJ, de Vries SJ, Kemmeren P, Huang A, Boelens R, Bonvin AM, Timmers HT, (2009) A comprehensive framework of E2-RING E3 interactions of the human ubiquitin-proteasome system. Mol Syst Biol 5: 295
115. Tatematsu K, Yoshimoto N, Okajima T, Tanizawa K, Kuroda S, (2008) Identification of ubiquitin ligase activity of RBCK1 and its inhibition by splice variant RBCK2 and protein kinase Cbeta. J Biol Chem 283: 11575-11585
116. Niwa J, Ishigaki S, Doyu M, Suzuki T, Tanaka K, Sobue G, (2001) A novel centrosomal ring-finger protein, dorfin, mediates ubiquitin ligase activity. Biochem Biophys Res Commun 281: 706-713 (Pubitemid 32917858)
117. Ito T, Niwa J, Hishikawa N, Ishigaki S, Doyu M, Sobue G, (2003) Dorfin localizes to Lewy bodies and ubiquitylates synphilin-1. J Biol Chem 278: 29106-29114 (Pubitemid 36935825)
118. Niwa J, Ishigaki S, Hishikawa N, Yamamoto M, Doyu M, Murata S, Tanaka K, Taniguchi N, Sobue G, (2002) Dorfin ubiquitylates mutant SOD1 and prevents mutant SOD1-mediated neurotoxicity. J Biol Chem 277: 36793-36798
119. Fortier JM, Kornbluth J, (2006) NK lytic-associated molecule, involved in NK cytotoxic function, is an E3 ligase. J Immunol 176: 6454-6463 (Pubitemid 43787827)
120. Ambrose EC, Kornbluth J, (2009) Downregulation of uridine-cytidine kinase like-1 decreases proliferation and enhances tumor susceptibility to lysis by apoptotic agents and natural killer cells. Apoptosis 14: 1227-1236
121. Ehrlund A, Anthonisen EH, Gustafsson N, Venteclef N, Robertson Remen K, Damdimopoulos AE, Galeeva A, Pelto-Huikko M, Lalli E, Steffensen KR, Gustafsson JA, Treuter E, (2009) E3 ubiquitin ligase RNF31 cooperates with DAX-1 in transcriptional repression of steroidogenesis. Mol Cell Biol 29: 2230-2242
122. Chuang TH, Ulevitch RJ, (2004) Triad3A, an E3 ubiquitin-protein ligase regulating Toll-like receptors. Nat Immunol 5: 495-502 (Pubitemid 38660461)
123. Kang HY, Yeh S, Fujimoto N, Chang C, (1999) Cloning and characterization of human prostate coactivator ARA54, a novel protein that associates with the androgen receptor. J Biol Chem 274: 8570-8576 (Pubitemid 29164648)
124. Ito K, Adachi S, Iwakami R, Yasuda H, Muto Y, Seki N, Okano Y, (2001) N-Terminally extended human ubiquitin-conjugating enzymes (E2s) mediate the ubiquitination of RING-finger proteins, ARA54 and RNF8. Eur J Biochem 268: 2725-2732 (Pubitemid 32853012)