Self-assembly Properties of a Model RING Domain

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2002 Jan 17

PMID 11792829

Citations 49

Authors

Alex Kentsis

Ronald E Gordon

Katherine L B Borden

Affiliations

Soon will be listed here.

Abstract

RING domains act in a variety of essential cellular processes but have no general function ascribed to them. Here, we observe that purified arenaviral protein Z, constituted almost entirely by its RING domain, self-assembles in vitro into spherical structures that resemble functional bodies formed by Z in infected cells. By using a variety of biophysical methods we provide a thermodynamic and kinetic framework for the RING-dependent self-assembly of Z. Assembly appears coupled to substantial conformational reorganization and changes in zinc coordination of site II of the RING. Thus, the rate-limiting nature of conformational reorganization observed in the folding of monomeric proteins can also apply to the assembly of macromolecular scaffolds. These studies describe a unique mechanism of nonfibrillar homogeneous self-assembly and suggest a general function of RINGs in the formation of macromolecular scaffolds that are positioned to integrate biochemical processes in cells.

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References

Di Simone C, Zandonatti M, Buchmeier M . Acidic pH triggers LCMV membrane fusion activity and conformational change in the glycoprotein spike. Virology. 1994; 198(2):455-65. DOI: 10.1006/viro.1994.1057. View

Quirion F, Gicquaud C . Changes in molar volume and heat capacity of actin upon polymerization. Biochem J. 1993; 295 ( Pt 3):671-2. PMC: 1134611. DOI: 10.1042/bj2950671. View

Di Simone C, Buchmeier M . Kinetics and pH dependence of acid-induced structural changes in the lymphocytic choriomeningitis virus glycoprotein complex. Virology. 1995; 209(1):3-9. DOI: 10.1006/viro.1995.1225. View

Mann C, Shao X, Matthews C . Characterization of the slow folding reactions of trp aporepressor from Escherichia coli by mutational analysis of prolines and catalysis by a peptidyl-prolyl isomerase. Biochemistry. 1995; 34(44):14573-80. DOI: 10.1021/bi00044a036. View

Makhatadze G, Privalov P . Energetics of protein structure. Adv Protein Chem. 1995; 47:307-425. DOI: 10.1016/s0065-3233(08)60548-3. View

Lobert S, Vulevic B, Correia J . Interaction of vinca alkaloids with tubulin: a comparison of vinblastine, vincristine, and vinorelbine. Biochemistry. 1996; 35(21):6806-14. DOI: 10.1021/bi953037i. View

Saurin A, Borden K, Boddy M, Freemont P . Does this have a familiar RING?. Trends Biochem Sci. 1996; 21(6):208-14. View

Demeler B, Saber H, Hansen J . Identification and interpretation of complexity in sedimentation velocity boundaries. Biophys J. 1997; 72(1):397-407. PMC: 1184330. DOI: 10.1016/S0006-3495(97)78680-6. View

Kelly J . Amyloid fibril formation and protein misassembly: a structural quest for insights into amyloid and prion diseases. Structure. 1997; 5(5):595-600. DOI: 10.1016/s0969-2126(97)00215-3. View

10.

Berg J, Godwin H . Lessons from zinc-binding peptides. Annu Rev Biophys Biomol Struct. 1997; 26:357-71. DOI: 10.1146/annurev.biophys.26.1.357. View

11.

Roehm P, Berg J . Sequential metal binding by the RING finger domain of BRCA1. Biochemistry. 1997; 36(33):10240-5. DOI: 10.1021/bi970863d. View

12.

Borden K, Campbell Dwyer E, Salvato M . An arenavirus RING (zinc-binding) protein binds the oncoprotein promyelocyte leukemia protein (PML) and relocates PML nuclear bodies to the cytoplasm. J Virol. 1998; 72(1):758-66. PMC: 109432. DOI: 10.1128/JVI.72.1.758-766.1998. View

13.

Brzovic P, Meza J, King M, Klevit R . The cancer-predisposing mutation C61G disrupts homodimer formation in the NH2-terminal BRCA1 RING finger domain. J Biol Chem. 1998; 273(14):7795-9. DOI: 10.1074/jbc.273.14.7795. View

14.

Borden K, Campbelldwyer E, Carlile G, Djavani M, Salvato M . Two RING finger proteins, the oncoprotein PML and the arenavirus Z protein, colocalize with the nuclear fraction of the ribosomal P proteins. J Virol. 1998; 72(5):3819-26. PMC: 109605. DOI: 10.1128/JVI.72.5.3819-3826.1998. View

15.

Miyake S, Lupher Jr M, Druker B, Band H . The tyrosine kinase regulator Cbl enhances the ubiquitination and degradation of the platelet-derived growth factor receptor alpha. Proc Natl Acad Sci U S A. 1998; 95(14):7927-32. PMC: 20906. DOI: 10.1073/pnas.95.14.7927. View

16.

Melnick A, Licht J . Deconstructing a disease: RARalpha, its fusion partners, and their roles in the pathogenesis of acute promyelocytic leukemia. Blood. 1999; 93(10):3167-215. View

17.

De Young L, Schmelzer C, Burton L . A common mechanism for recombinant human NGF, BDNF, NT-3, and murine NGF slow unfolding. Protein Sci. 1999; 8(11):2513-8. PMC: 2144210. DOI: 10.1110/ps.8.11.2513. View

18.

Peng H, Begg G, Schultz D, Friedman J, Jensen D, Speicher D . Reconstitution of the KRAB-KAP-1 repressor complex: a model system for defining the molecular anatomy of RING-B box-coiled-coil domain-mediated protein-protein interactions. J Mol Biol. 2000; 295(5):1139-62. DOI: 10.1006/jmbi.1999.3402. View

19.

Campbell Dwyer E, Lai H, Macdonald R, Salvato M, Borden K . The lymphocytic choriomeningitis virus RING protein Z associates with eukaryotic initiation factor 4E and selectively represses translation in a RING-dependent manner. J Virol. 2000; 74(7):3293-300. PMC: 111830. DOI: 10.1128/jvi.74.7.3293-3300.2000. View

20.

Schlessinger J . Cell signaling by receptor tyrosine kinases. Cell. 2000; 103(2):211-25. DOI: 10.1016/s0092-8674(00)00114-8. View