TRIAD1 and HHARI Bind to and Are Activated by Distinct Neddylated Cullin-RING Ligase Complexes

Overview

Journal EMBO J

Specialties Biotechnology
Molecular Biology

Date 2013 Oct 1

PMID 24076655

Citations 59

Authors

Ian R Kelsall

David M Duda

Jennifer L Olszewski

Kay Hofmann

Axel Knebel

Frederic Langevin

Nicola Wood

Melanie Wightman

Brenda A Schulman

Arno F Alpi

Affiliations

Soon will be listed here.

Abstract

RING (Really Interesting New Gene)-in-between-RING (RBR) enzymes are a distinct class of E3 ubiquitin ligases possessing a cluster of three zinc-binding domains that cooperate to catalyse ubiquitin transfer. The regulation and biological function for most members of the RBR ligases is not known, and all RBR E3s characterized to date are auto-inhibited for in vitro ubiquitylation. Here, we show that TRIAD1 and HHARI, two members of the Ariadne subfamily ligases, associate with distinct neddylated Cullin-RING ligase (CRL) complexes. In comparison to the modest E3 ligase activity displayed by isolated TRIAD1 or HHARI, binding of the cognate neddylated CRL to TRIAD1 or HHARI greatly stimulates RBR ligase activity in vitro, as determined by auto-ubiquitylation, their ability to stimulate dissociation of a thioester-linked UBCH7∼ubiquitin intermediate, and reactivity with ubiquitin-vinyl methyl ester. Moreover, genetic evidence shows that RBR ligase activity impacts both the levels and activities of neddylated CRLs in vivo. Cumulatively, our work proposes a conserved mechanism of CRL-induced Ariadne RBR ligase activation and further suggests a reciprocal role of this special class of RBRs as regulators of distinct CRLs.

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References

Elmehdawi F, Wheway G, Szymanska K, Adams M, High A, Johnson C . Human Homolog of Drosophila Ariadne (HHARI) is a marker of cellular proliferation associated with nuclear bodies. Exp Cell Res. 2012; 319(3):161-72. DOI: 10.1016/j.yexcr.2012.10.002. View

Pierce N, Lee J, Liu X, Sweredoski M, Graham R, Larimore E . Cand1 promotes assembly of new SCF complexes through dynamic exchange of F box proteins. Cell. 2013; 153(1):206-15. PMC: 3656483. DOI: 10.1016/j.cell.2013.02.024. View

Lin A, Ebert G, Ow Y, Preston S, Toe J, Cooney J . ARIH2 is essential for embryogenesis, and its hematopoietic deficiency causes lethal activation of the immune system. Nat Immunol. 2012; 14(1):27-33. DOI: 10.1038/ni.2478. View

Katoh K, Misawa K, Kuma K, Miyata T . MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res. 2002; 30(14):3059-66. PMC: 135756. DOI: 10.1093/nar/gkf436. View

Huang D, Ayrault O, Hunt H, Taherbhoy A, Duda D, Scott D . E2-RING expansion of the NEDD8 cascade confers specificity to cullin modification. Mol Cell. 2009; 33(4):483-95. PMC: 2725360. DOI: 10.1016/j.molcel.2009.01.011. View

Spratt D, Martinez-Torres R, Noh Y, Mercier P, Manczyk N, Barber K . A molecular explanation for the recessive nature of parkin-linked Parkinson's disease. Nat Commun. 2013; 4:1983. PMC: 3709501. DOI: 10.1038/ncomms2983. View

Wenzel D, Lissounov A, Brzovic P, Klevit R . UBCH7 reactivity profile reveals parkin and HHARI to be RING/HECT hybrids. Nature. 2011; 474(7349):105-8. PMC: 3444301. DOI: 10.1038/nature09966. View

Scott D, Monda J, Grace C, Duda D, Kriwacki R, Kurz T . A dual E3 mechanism for Rub1 ligation to Cdc53. Mol Cell. 2010; 39(5):784-96. PMC: 3001161. DOI: 10.1016/j.molcel.2010.08.030. View

Lyapina S, Cope G, Serino G, Tsuge T, Zhou C, Wolf D . Promotion of NEDD-CUL1 conjugate cleavage by COP9 signalosome. Science. 2001; 292(5520):1382-5. DOI: 10.1126/science.1059780. View

10.

Liakopoulos D, Doenges G, Matuschewski K, Jentsch S . A novel protein modification pathway related to the ubiquitin system. EMBO J. 1998; 17(8):2208-14. PMC: 1170565. DOI: 10.1093/emboj/17.8.2208. View

11.

Stieglitz B, Morris-Davies A, Koliopoulos M, Christodoulou E, Rittinger K . LUBAC synthesizes linear ubiquitin chains via a thioester intermediate. EMBO Rep. 2012; 13(9):840-6. PMC: 3432797. DOI: 10.1038/embor.2012.105. View

12.

Deshaies R, Joazeiro C . RING domain E3 ubiquitin ligases. Annu Rev Biochem. 2009; 78:399-434. DOI: 10.1146/annurev.biochem.78.101807.093809. View

13.

Kelsall I, Langenick J, MacKay C, Patel K, Alpi A . The Fanconi anaemia components UBE2T and FANCM are functionally linked to nucleotide excision repair. PLoS One. 2012; 7(5):e36970. PMC: 3352854. DOI: 10.1371/journal.pone.0036970. View

14.

Smit J, Monteferrario D, Noordermeer S, van Dijk W, van der Reijden B, Sixma T . The E3 ligase HOIP specifies linear ubiquitin chain assembly through its RING-IBR-RING domain and the unique LDD extension. EMBO J. 2012; 31(19):3833-44. PMC: 3463842. DOI: 10.1038/emboj.2012.217. View

15.

Kleiger G, Saha A, Lewis S, Kuhlman B, Deshaies R . Rapid E2-E3 assembly and disassembly enable processive ubiquitylation of cullin-RING ubiquitin ligase substrates. Cell. 2009; 139(5):957-68. PMC: 2804849. DOI: 10.1016/j.cell.2009.10.030. View

16.

Lee D, Peggie M, Deak M, Toth R, Gage Z, Wood N . The Dac-tag, an affinity tag based on penicillin-binding protein 5. Anal Biochem. 2012; 428(1):64-72. DOI: 10.1016/j.ab.2012.06.007. View

17.

den Besten W, Verma R, Kleiger G, Oania R, Deshaies R . NEDD8 links cullin-RING ubiquitin ligase function to the p97 pathway. Nat Struct Mol Biol. 2012; 19(5):511-6, S1. PMC: 3348432. DOI: 10.1038/nsmb.2269. View

18.

Soding J, Biegert A, Lupas A . The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 2005; 33(Web Server issue):W244-8. PMC: 1160169. DOI: 10.1093/nar/gki408. View

19.

Wu S, Zhu W, Nhan T, Toth J, Petroski M, Wolf D . CAND1 controls in vivo dynamics of the cullin 1-RING ubiquitin ligase repertoire. Nat Commun. 2013; 4:1642. PMC: 3637025. DOI: 10.1038/ncomms2636. View

20.

Marteijn J, van Emst L, Erpelinck-Verschueren C, Nikoloski G, Menke A, de Witte T . The E3 ubiquitin-protein ligase Triad1 inhibits clonogenic growth of primary myeloid progenitor cells. Blood. 2005; 106(13):4114-23. DOI: 10.1182/blood-2005-04-1450. View