NAD+ cleavage activity by animal and plant TIR domains in cell death pathways

Shane Horsefield; Hayden Burdett; Xiaoxiao Zhang; Mohammad K. Manik; Yun Shi; Jian Chen; Tiancong Qi; Jonathan Gilley; Jhih Siang Lai; Maxwell X. Rank; Lachlan W. Casey; Weixi Gu; Daniel J. Ericsson; Gabriel Foley; Robert O. Hughes; Todd Bosanac; Mark Von Itzstein; John P. Rathjen; Jeffrey D. Nanson; Mikael Boden; Ian B. Dry; Simon J. Williams; Brian J. Staskawicz; Michael P. Coleman; Thomas Ve; Peter N. Dodds; Bostjan Kobe

doi:10.1126/science.aax1911

NAD+ cleavage activity by animal and plant TIR domains in cell death pathways

Shane Horsefield, Hayden Burdett, Xiaoxiao Zhang, Mohammad K. Manik, Yun Shi, Jian Chen, Tiancong Qi, Jonathan Gilley, Jhih Siang Lai, Maxwell X. Rank, Lachlan W. Casey, Weixi Gu, Daniel J. Ericsson, Gabriel Foley, Robert O. Hughes, Todd Bosanac, Mark Von Itzstein, John P. Rathjen, Jeffrey D. Nanson, Mikael BodenIan B. Dry, Simon J. Williams, Brian J. Staskawicz, Michael P. Coleman, Thomas Ve^*, Peter N. Dodds, Bostjan Kobe

^*Corresponding author for this work

Research output: Contribution to journal › Article › peer-review

333 Citations (Scopus)

Abstract

SARM1 (sterile alpha and TIR motif containing 1) is responsible for depletion of nicotinamide adenine dinucleotide in its oxidized form (NAD+) during Wallerian degeneration associated with neuropathies. Plant nucleotide-binding leucine-rich repeat (NLR) immune receptors recognize pathogen effector proteins and trigger localized cell death to restrict pathogen infection. Both processes depend on closely related Toll/interleukin-1 receptor (TIR) domains in these proteins, which, as we show, feature self-association-dependent NAD+ cleavage activity associated with cell death signaling. We further show that SARM1 SAM (sterile alpha motif) domains form an octamer essential for axon degeneration that contributes to TIR domain enzymatic activity. The crystal structures of ribose and NADP+ (the oxidized form of nicotinamide adenine dinucleotide phosphate) complexes of SARM1 and plant NLR RUN1 TIR domains, respectively, reveal a conserved substrate binding site. NAD+ cleavage by TIR domains is therefore a conserved feature of animal and plant cell death signaling pathways.

Original language	English
Pages (from-to)	793-799
Number of pages	7
Journal	Science
Volume	365
Issue number	6455
DOIs	https://doi.org/10.1126/science.aax1911
Publication status	Published - 23 Aug 2019

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Horsefield, S., Burdett, H., Zhang, X., Manik, M. K., Shi, Y., Chen, J., Qi, T., Gilley, J., Lai, J. S., Rank, M. X., Casey, L. W., Gu, W., Ericsson, D. J., Foley, G., Hughes, R. O., Bosanac, T., Von Itzstein, M., Rathjen, J. P., Nanson, J. D., ... Kobe, B. (2019). NAD+ cleavage activity by animal and plant TIR domains in cell death pathways. Science, 365(6455), 793-799. https://doi.org/10.1126/science.aax1911

@article{f0ce4c183e4b4d25bfe410be4eea9849,

title = "NAD+ cleavage activity by animal and plant TIR domains in cell death pathways",

abstract = "SARM1 (sterile alpha and TIR motif containing 1) is responsible for depletion of nicotinamide adenine dinucleotide in its oxidized form (NAD+) during Wallerian degeneration associated with neuropathies. Plant nucleotide-binding leucine-rich repeat (NLR) immune receptors recognize pathogen effector proteins and trigger localized cell death to restrict pathogen infection. Both processes depend on closely related Toll/interleukin-1 receptor (TIR) domains in these proteins, which, as we show, feature self-association-dependent NAD+ cleavage activity associated with cell death signaling. We further show that SARM1 SAM (sterile alpha motif) domains form an octamer essential for axon degeneration that contributes to TIR domain enzymatic activity. The crystal structures of ribose and NADP+ (the oxidized form of nicotinamide adenine dinucleotide phosphate) complexes of SARM1 and plant NLR RUN1 TIR domains, respectively, reveal a conserved substrate binding site. NAD+ cleavage by TIR domains is therefore a conserved feature of animal and plant cell death signaling pathways.",

author = "Shane Horsefield and Hayden Burdett and Xiaoxiao Zhang and Manik, {Mohammad K.} and Yun Shi and Jian Chen and Tiancong Qi and Jonathan Gilley and Lai, {Jhih Siang} and Rank, {Maxwell X.} and Casey, {Lachlan W.} and Weixi Gu and Ericsson, {Daniel J.} and Gabriel Foley and Hughes, {Robert O.} and Todd Bosanac and {Von Itzstein}, Mark and Rathjen, {John P.} and Nanson, {Jeffrey D.} and Mikael Boden and Dry, {Ian B.} and Williams, {Simon J.} and Staskawicz, {Brian J.} and Coleman, {Michael P.} and Thomas Ve and Dodds, {Peter N.} and Bostjan Kobe",

note = "Publisher Copyright: {\textcopyright} The Authors, some rights reserved.",

year = "2019",

month = aug,

day = "23",

doi = "10.1126/science.aax1911",

language = "English",

volume = "365",

pages = "793--799",

journal = "Science",

issn = "0036-8075",

publisher = "American Association for the Advancement of Science",

number = "6455",

}

Horsefield, S, Burdett, H, Zhang, X, Manik, MK, Shi, Y, Chen, J, Qi, T, Gilley, J, Lai, JS, Rank, MX, Casey, LW, Gu, W, Ericsson, DJ, Foley, G, Hughes, RO, Bosanac, T, Von Itzstein, M, Rathjen, JP, Nanson, JD, Boden, M, Dry, IB, Williams, SJ, Staskawicz, BJ, Coleman, MP, Ve, T, Dodds, PN & Kobe, B 2019, 'NAD+ cleavage activity by animal and plant TIR domains in cell death pathways', Science, vol. 365, no. 6455, pp. 793-799. https://doi.org/10.1126/science.aax1911

TY - JOUR

T1 - NAD+ cleavage activity by animal and plant TIR domains in cell death pathways

AU - Horsefield, Shane

AU - Burdett, Hayden

AU - Zhang, Xiaoxiao

AU - Manik, Mohammad K.

AU - Shi, Yun

AU - Chen, Jian

AU - Qi, Tiancong

AU - Gilley, Jonathan

AU - Lai, Jhih Siang

AU - Rank, Maxwell X.

AU - Casey, Lachlan W.

AU - Gu, Weixi

AU - Ericsson, Daniel J.

AU - Foley, Gabriel

AU - Hughes, Robert O.

AU - Bosanac, Todd

AU - Von Itzstein, Mark

AU - Rathjen, John P.

AU - Nanson, Jeffrey D.

AU - Boden, Mikael

AU - Dry, Ian B.

AU - Williams, Simon J.

AU - Staskawicz, Brian J.

AU - Coleman, Michael P.

AU - Ve, Thomas

AU - Dodds, Peter N.

AU - Kobe, Bostjan

PY - 2019/8/23

Y1 - 2019/8/23

N2 - SARM1 (sterile alpha and TIR motif containing 1) is responsible for depletion of nicotinamide adenine dinucleotide in its oxidized form (NAD+) during Wallerian degeneration associated with neuropathies. Plant nucleotide-binding leucine-rich repeat (NLR) immune receptors recognize pathogen effector proteins and trigger localized cell death to restrict pathogen infection. Both processes depend on closely related Toll/interleukin-1 receptor (TIR) domains in these proteins, which, as we show, feature self-association-dependent NAD+ cleavage activity associated with cell death signaling. We further show that SARM1 SAM (sterile alpha motif) domains form an octamer essential for axon degeneration that contributes to TIR domain enzymatic activity. The crystal structures of ribose and NADP+ (the oxidized form of nicotinamide adenine dinucleotide phosphate) complexes of SARM1 and plant NLR RUN1 TIR domains, respectively, reveal a conserved substrate binding site. NAD+ cleavage by TIR domains is therefore a conserved feature of animal and plant cell death signaling pathways.

AB - SARM1 (sterile alpha and TIR motif containing 1) is responsible for depletion of nicotinamide adenine dinucleotide in its oxidized form (NAD+) during Wallerian degeneration associated with neuropathies. Plant nucleotide-binding leucine-rich repeat (NLR) immune receptors recognize pathogen effector proteins and trigger localized cell death to restrict pathogen infection. Both processes depend on closely related Toll/interleukin-1 receptor (TIR) domains in these proteins, which, as we show, feature self-association-dependent NAD+ cleavage activity associated with cell death signaling. We further show that SARM1 SAM (sterile alpha motif) domains form an octamer essential for axon degeneration that contributes to TIR domain enzymatic activity. The crystal structures of ribose and NADP+ (the oxidized form of nicotinamide adenine dinucleotide phosphate) complexes of SARM1 and plant NLR RUN1 TIR domains, respectively, reveal a conserved substrate binding site. NAD+ cleavage by TIR domains is therefore a conserved feature of animal and plant cell death signaling pathways.

UR - http://www.scopus.com/inward/record.url?scp=85071359553&partnerID=8YFLogxK

U2 - 10.1126/science.aax1911

DO - 10.1126/science.aax1911

M3 - Article

SN - 0036-8075

VL - 365

SP - 793

EP - 799

JO - Science

JF - Science

IS - 6455

ER -

NAD+ cleavage activity by animal and plant TIR domains in cell death pathways

Abstract

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