Structural studies of an antinecroptosis viral:human functional heteroamyloid M45:RIPK3 using SSNMR

C Chengming He (Department of Chemistry, Columbia University) N Nikhil R. Varghese (School of Medical Sciences and Sydney Nano Institute, University of Sydney) E Eric G. Keeler (Department of Chemistry, Columbia University) C Chi L. L. Pham (School of Medical Sciences and Sydney Nano Institute, University of Sydney) T Teng Xie (Institute of Quantitative Biology, Zhejiang University) B Brayden Williams (School of Medical Sciences and Sydney Nano Institute, University of Sydney) S Stephan Tetter (Laboratory of Organic Chemistry, ETH Zurich) C Crystal Semaan (School of Medical Sciences and Sydney Nano Institute, University of Sydney) K Karyn L. Wilde (National Deuteration Facility, Australian Nuclear Science and Technology Organization) S Simon H. J. Brown (School of Chemistry and Molecular Bioscience, Molecular Horizons, and Australian Research Council Centre for Cryo-electron Microscopy of Membrane Proteins, University of Wollongong) J James C. Bouwer (Australian Research Council Centre for Cryo-electron Microscopy of Membrane Proteins, University of Wollongong) Y Yann Gambin (Department of Molecular Medicine and European Molecular Biology Laboratory Australia Node in Single Molecule Science, School of Biomedical Sciences, University of New South Wales) E Emma Sierecki (Department of Molecular Medicine and European Molecular Biology Laboratory Australia Node in Single Molecule Science, School of Biomedical Sciences, University of New South Wales) M Megan Steain (School of Medical Sciences and Sydney Nano Institute, University of Sydney) R Ruhong Zhou M Margaret Sunde (School of Medical Sciences and Sydney Nano Institute, University of Sydney) A Ann E. McDermott (Department of Chemistry, Columbia University)

Abstract

The formation of RIP-homotypic interaction motif (RHIM)-based heteromeric amyloid assemblies between effector proteins such as receptor-interacting protein kinases 1, Z-DNA Binding Protein 1, or TRIF and the kinase RIPK3 serves as regulating signals for the necroptosis process, a key element of innate immune defense. Murine cytomegalovirus expresses the M45-encoded viral inhibitor of RIP activation which inhibits necroptosis in a RHIM-dependent manner. A pivotal question is how viral M45 forms heteroamyloids with RIPK3 to effectively create an inhibitory assembly. We report a high-resolution structure of the M45:RIPK3 complex where M45 and RIPK3 alternately stack in an amyloid-state structure. Mutagenesis of the residues flanking the IQIG tetrad in M45 results in specific impacts on coassembly with RIPK3, indicating an extended interface in the heteromeric fibrils. Other key interactions support the formation of stable viral:host fibrils. The M45:RIPK3 heteroamyloid is likely to act as an antinecroptotic signal by competing with formation of other pronecroptotic species and introducing a barrier to RIPK3 autophosphorylation.

Article Details

Volume / Issue Vol. 123, Issue 18
Published May 05, 2026
ISSN 0027-8424
Publisher National Academy of Sciences

Authors (17)

C

Chengming He

Department of Chemistry, Columbia University

N

Nikhil R. Varghese

School of Medical Sciences and Sydney Nano Institute, University of Sydney

E

Eric G. Keeler

Department of Chemistry, Columbia University

C

Chi L. L. Pham

School of Medical Sciences and Sydney Nano Institute, University of Sydney

T

Teng Xie

Institute of Quantitative Biology, Zhejiang University

B

Brayden Williams

School of Medical Sciences and Sydney Nano Institute, University of Sydney

S

Stephan Tetter

Laboratory of Organic Chemistry, ETH Zurich

C

Crystal Semaan

School of Medical Sciences and Sydney Nano Institute, University of Sydney

K

Karyn L. Wilde

National Deuteration Facility, Australian Nuclear Science and Technology Organization

S

Simon H. J. Brown

School of Chemistry and Molecular Bioscience, Molecular Horizons, and Australian Research Council Centre for Cryo-electron Microscopy of Membrane Proteins, University of Wollongong

J

James C. Bouwer

Australian Research Council Centre for Cryo-electron Microscopy of Membrane Proteins, University of Wollongong

Y

Yann Gambin

Department of Molecular Medicine and European Molecular Biology Laboratory Australia Node in Single Molecule Science, School of Biomedical Sciences, University of New South Wales

E

Emma Sierecki

Department of Molecular Medicine and European Molecular Biology Laboratory Australia Node in Single Molecule Science, School of Biomedical Sciences, University of New South Wales

M

Megan Steain

School of Medical Sciences and Sydney Nano Institute, University of Sydney

R

Ruhong Zhou

M

Margaret Sunde

School of Medical Sciences and Sydney Nano Institute, University of Sydney

A

Ann E. McDermott

Department of Chemistry, Columbia University