Abstract
Main conclusion
A conserved cysteine residue (C266)-mediated homo-dimerization of SIE3 is required for the ubiquitination and degradation of SIP1 transcription factor in Lotus japonicas
Abstract
CTLH/CRA/RING-containing proteins have been shown to possess E3-ligase activities and are crucial for the regulation of numerous cellular signaling pathways. In our previous studies, SIE3 (SymRK-Interacting E3 ubiquitin ligase), a CTLH/CRA/RING-containing protein from Lotus japonicus, has been shown to associate with both Symbiosis Receptor Kinase (SymRK) and SIP1 (SymRK interacting protein 1) transcription factor, and ubiquitinate SymRK (Yuan et al. Plant Physiol 160 (1):106–117, 2012; Feng et al. Front Plant Sci 11: 795, 2020). Besides, we previously also demonstrated that the residue, cysteine-266 in the CRA (CT11-RanBPM) domain is required for homodimerization of SIE3 and cysteine-266 residue-mediated homodimerization is important for the symbiosic function of SIE3 (Feng et al. 2020). In this report, SIE3 was shown to induce the ubiquitination and degradation of SIP1. The cysteine-266 residue is essential for the E3-ligase activity and is highly conserved in the SIE3-like proteins. Our works refined the working model that homodimerization of SIE3 is required for ubiquitin-related degradation of SIP1 and found a conserved cysteine residue plays a key role in the activity of a plant dimeric E3 ligase.
Abbreviations
- CRA:
-
CT11-RanBPM
- CTLH:
-
C-terminal to LisH
- GID:
-
Glucose-induced degradation deficient
- SIE3:
-
SymRK-Interacting E3 ubiquitin ligase
- SIP1:
-
SymRK interacting protein 1
- SymRK:
-
Symbiosis Receptor Kinase
References
Blanco-Touriñán N, Legris M, Minguet EG, Costigliolo-Rojas C, Nohales MA, Iniesto E, García-Leόn M, Pacín M, Heucken N, Blomeier T, Locascio A, Černý M, Esteve-Bruna D, Díez-Díaz M, Brzobohatý B, Frerigmann H, Zurbriggen MD, Kay SA, Rubio V, Blázquez MA, Casal JJ, Alabadí D (2020) COP1 destabilizes DELLA proteins in Arabidopsis. Proc Natl Acad Sci USA 117(24):13792–13799. https://doi.org/10.1073/pnas.1907969117
Brzovic PS, Rajagopal P, Hoyt DW, King M-C, Klevit RE (2001) Structure of a BRCA1–BARD1 heterodimeric RING–RING complex. Nat Struct Biol 8(10):833–837. https://doi.org/10.1038/nsb1001-833
Buchwald G, van der Stoop P, Weichenrieder O, Perrakis A, van Lohuizen M, Sixma TK (2006) Structure and E3-ligase activity of the Ring-Ring complex of polycomb proteins Bmi1 and Ring1b. EMBO J 25(11):2465–2474. https://doi.org/10.1038/sj.emboj.7601144
Deshaies RJ, Joazeiro CAP (2009) RING domain E3 ubiquitin ligases. Annu Rev Biochem 78:399–434. https://doi.org/10.1146/annurev.biochem.78.101807.093809
Feng Y, Wu P, Fu W, Peng L, Zhu H, Cao Y, Zhou X, Hong Z, Zhang Z, Yuan S (2020) The Lotus japonicus ubiquitin ligase SIE3 interacts with the transcription factor SIP1 and forms a homodimer. Front Plant Sci 11:795. https://doi.org/10.3389/fpls.2020.00795
Grabbe C, Husnjak K, Dikic I (2011) The spatial and temporal organization of ubiquitin networks. Nat Rev Mol Cell Biol 12(5):295–307. https://doi.org/10.1038/nrm3099
Han Y, Sun J, Yang J, Tan Z, Luo J, Lu D (2017) Reconstitution of the plant ubiquitination cascade in bacteria using a synthetic biology approach. Plant J 91(4):766–776. https://doi.org/10.1111/tpj.13603
Huffman N, Palmieri D, Coppola V (2019) The CTLH complex in cancer cell plasticity. J Oncol 2019:4216750. https://doi.org/10.1155/2019/4216750
Kosztyu P, Slaninová I, Valčíková B, Verlande A, Müller P, Paleček JJ, Uldrijan S (2019) A single conserved amino acid residue as a critical context-specific determinant of the differential ability of mdm2 and mdmX RING domains to dimerize. Front Physiol 10:390. https://doi.org/10.3389/fphys.2019.00390
Lampert F, Stafa D, Goga A, Soste MV, Gilberto S, Olieric N, Picotti P, Stoffel M, Peter M (2018) The multi-subunit GID/CTLH E3 ubiquitin ligase promotes cell proliferation and targets the transcription factor Hbp1 for degradation. eLife 7:e35528. https://doi.org/10.7554/eLife.35528
Li X, Elmira E, Rohondia S, Wang J, Liu J, Dou QP (2018) A patent review of the ubiquitin ligase system: 2015–2018. Expert Opin Therap Patents 28(12):919–937. https://doi.org/10.1080/13543776.2018.1549229
Liew Chu W, Sun H, Hunter T, Day Catherine L (2010) RING domain dimerization is essential for RNF4 function. Biochem J 431(1):23–29. https://doi.org/10.1042/bj20100957
Linke K, Mace PD, Smith CA, Vaux DL, Silke J, Day CL (2008) Structure of the MDM2/MDMX RING domain heterodimer reveals dimerization is required for their ubiquitylation in trans. Cell Death Differ 15(5):841–848. https://doi.org/10.1038/sj.cdd.4402309
Liu H, Pfirrmann T (2019) The Gid-complex: an emerging player in the ubiquitin ligase league. Biol Chem 400(11):1429–1441. https://doi.org/10.1515/hsz-2019-0139
Liu L, Zhang Y, Tang S, Zhao Q, Zhang Z, Zhang H, Dong L, Guo H, Xie Q (2010) An efficient system to detect protein ubiquitination by agroinfiltration in Nicotiana benthamiana. Plant J 61(5):893–903. https://doi.org/10.1111/j.1365-313X.2009.04109.x
Liu H, Ding J, Köhnlein K, Urban N, Ori A, Villavicencio-Lorini P, Walentek P, Klotz LO, Hollemann T, Pfirrmann T (2020) The GID ubiquitin ligase complex is a regulator of AMPK activity and organismal lifespan. Autophagy 16(9):1618–1634. https://doi.org/10.1080/15548627.2019.1695399
Mace PD, Linke K, Feltham R, Schumacher F-R, Smith CA, Vaux DL, Silke J, Day CL (2008) Structures of the cIAP2 RING domain reveal conformational changes associated with ubiquitin-conjugating enzyme (E2) recruitment. J Biol Chem 283(46):31633–31640. https://doi.org/10.1074/jbc.M804753200
Morris JR, Keep NH, Solomon E (2002) Identification of residues required for the interaction of BARD1 with BRCA1. J Biol Chem 277(11):9382–9386. https://doi.org/10.1074/jbc.M109249200
Nakamura T, Yamada KD, Tomii K, Katoh K (2018) Parallelization of MAFFT for large-scale multiple sequence alignments. Bioinformatics 34(14):2490–2492. https://doi.org/10.1093/bioinformatics/bty121
Nakatani Y, Kleffmann T, Linke K, Condon SM, Hinds MG, Day CL (2013) Regulation of ubiquitin transfer by XIAP, a dimeric RING E3 ligase. Biochem J 450(3):629–638. https://doi.org/10.1042/bj20121702
Petroski MD, Deshaies RJ (2005) Function and regulation of cullin–RING ubiquitin ligases. Nat Rev Mol Cell Biol 6(1):9–20. https://doi.org/10.1038/nrm1547
Plechanovová A, Jaffray EG, McMahon SA, Johnson KA, Navrátilová I, Naismith JH, Hay RT (2011) Mechanism of ubiquitylation by dimeric RING ligase RNF4. Nat Struct Mol Biol 18(9):1052–1059. https://doi.org/10.1038/nsmb.2108
Robert X, Gouet P (2014) Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Res 42 (Web Server issue):W320–324. https://doi.org/10.1093/nar/gku316
Salemi LM, Maitland MER, McTavish CJ, Schild-Poulter C (2017) Cell signalling pathway regulation by RanBPM: molecular insights and disease implications. Open Biol 7:6. https://doi.org/10.1098/rsob.170081
Santt O, Pfirrmann T, Braun B, Juretschke J, Kimmig P, Scheel H, Hofmann K, Thumm M, Wolf DH (2008) The yeast GID complex, a novel ubiquitin ligase (E3) involved in the regulation of carbohydrate metabolism. Mol Biol Cell 19(8):3323–3333. https://doi.org/10.1091/mbc.e08-03-0328
Vander Kooi CW, Ohi MD, Rosenberg JA, Oldham ML, Newcomer ME, Gould KL, Chazin WJ (2006) The Prp19 U-box crystal structure suggests a common dimeric architecture for a class of oligomeric E3 ubiquitin ligases. Biochemistry 45(1):121–130. https://doi.org/10.1021/bi051787e
Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G, Gumienny R, Heer FT, de Beer TAP, Rempfer C, Bordoli L, Lepore R, Schwede T (2018) SWISS-MODEL: homology modelling of protein structures and complexes. Nucl Acids Res 46(W1):W296-w303. https://doi.org/10.1093/nar/gky427
Xie Q, Guo H-S, Dallman G, Fang S, Weissman AM, Chua N-H (2002) SINAT5 promotes ubiquitin-related degradation of NAC1 to attenuate auxin signals. Nature 419(6903):167–170. https://doi.org/10.1038/nature00998
Yao F, Zhou Z, Kim J, Hang Q, Xiao Z, Ton BN, Chang L, Liu N, Zeng L, Wang W, Wang Y, Zhang P, Hu X, Su X, Liang H, Sun Y, Ma L (2018) SKP2- and OTUD1-regulated non-proteolytic ubiquitination of YAP promotes YAP nuclear localization and activity. Nat Commun 9(1):2269. https://doi.org/10.1038/s41467-018-04620-y
Yin Q, Lin S-C, Lamothe B, Lu M, Lo Y-C, Hura G, Zheng L, Rich RL, Campos AD, Myszka DG, Lenardo MJ, Darnay BG, Wu H (2009) E2 interaction and dimerization in the crystal structure of TRAF6. Nat Struct Mol Biol 16(6):658–666. https://doi.org/10.1038/nsmb.1605
Yuan S, Zhu H, Gou H, Fu W, Liu L, Chen T, Ke D, Kang H, Xie Q, Hong Z, Zhang Z (2012) A ubiquitin ligase of symbiosis receptor kinase involved in nodule organogenesis. Plant Physiol 160(1):106–117. https://doi.org/10.1104/pp.112.199000
Acknowledgements
This work was supported by funds from the National Key R&D Program of China (2019YFA0904703), the National Natural Science Foundation of China (Grant no. 32071964), and the Basic scientific research service fee special of the Central Scientific Research Institute (1610172018001).
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SY and YC designed this work; SY wrote the manuscript; PW, YF and ZZ performed most of the experiments and analysis.
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Wu, P., Feng, Y., Zou, Z. et al. Critical role of cysteine-266 of SIE3 in regulating the ubiquitination and degradation of SIP1 transcription factor in Lotus japonicus. Planta 253, 126 (2021). https://doi.org/10.1007/s00425-021-03647-8
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DOI: https://doi.org/10.1007/s00425-021-03647-8