Literature DB >> 34796871

Enrichment of SARM1 alleles encoding variants with constitutively hyperactive NADase in patients with ALS and other motor nerve disorders.

Jonathan Gilley1, Oscar Jackson1, Menelaos Pipis2, Mehrdad A Estiar3,4, Ammar Al-Chalabi5,6, Matt C Danzi7, Kristel R van Eijk8, Stephen A Goutman9, Matthew B Harms10, Henry Houlden2, Alfredo Iacoangeli5,11,12, Julia Kaye13, Leandro Lima13,14, John Ravits15, Guy A Rouleau3,4,16, Rebecca Schüle17, Jishu Xu17, Stephan Züchner7, Johnathan Cooper-Knock18, Ziv Gan-Or3,4,16, Mary M Reilly2, Michael P Coleman1.   

Abstract

SARM1, a protein with critical NADase activity, is a central executioner in a conserved programme of axon degeneration. We report seven rare missense or in-frame microdeletion human SARM1 variant alleles in patients with amyotrophic lateral sclerosis (ALS) or other motor nerve disorders that alter the SARM1 auto-inhibitory ARM domain and constitutively hyperactivate SARM1 NADase activity. The constitutive NADase activity of these seven variants is similar to that of SARM1 lacking the entire ARM domain and greatly exceeds the activity of wild-type SARM1, even in the presence of nicotinamide mononucleotide (NMN), its physiological activator. This rise in constitutive activity alone is enough to promote neuronal degeneration in response to otherwise non-harmful, mild stress. Importantly, these strong gain-of-function alleles are completely patient-specific in the cohorts studied and show a highly significant association with disease at the single gene level. These findings of disease-associated coding variants that alter SARM1 function build on previously reported genome-wide significant association with ALS for a neighbouring, more common SARM1 intragenic single nucleotide polymorphism (SNP) to support a contributory role of SARM1 in these disorders. A broad phenotypic heterogeneity and variable age-of-onset of disease among patients with these alleles also raises intriguing questions about the pathogenic mechanism of hyperactive SARM1 variants.
© 2021, Gilley et al.

Entities:  

Keywords:  ALS; NADase; SARM1; genetics; genomics; human; neuroscience; risk allele

Mesh:

Substances:

Year:  2021        PMID: 34796871      PMCID: PMC8735862          DOI: 10.7554/eLife.70905

Source DB:  PubMed          Journal:  Elife        ISSN: 2050-084X            Impact factor:   8.713


  68 in total

1.  Homozygous NMNAT2 mutation in sisters with polyneuropathy and erythromelalgia.

Authors:  Peter Huppke; Eike Wegener; Jonathan Gilley; Carlo Angeletti; Ingo Kurth; Joost P H Drenth; Christine Stadelmann; Alonso Barrantes-Freer; Wolfgang Brück; Holger Thiele; Peter Nürnberg; Jutta Gärtner; Giuseppe Orsomando; Michael P Coleman
Journal:  Exp Neurol       Date:  2019-05-24       Impact factor: 5.330

2.  The SARM1 Toll/Interleukin-1 Receptor Domain Possesses Intrinsic NAD+ Cleavage Activity that Promotes Pathological Axonal Degeneration.

Authors:  Kow Essuman; Daniel W Summers; Yo Sasaki; Xianrong Mao; Aaron DiAntonio; Jeffrey Milbrandt
Journal:  Neuron       Date:  2017-03-22       Impact factor: 17.173

3.  Familial ALS with extreme phenotypic variability due to the I113T SOD1 mutation.

Authors:  Glenn Lopate; Robert H Baloh; Muhammad T Al-Lozi; Timothy M Miller; J Americo Fernandes Filho; Oliver Ni; Alison Leston; Julaine Florence; Jeanine Schierbecker; Peggy Allred
Journal:  Amyotroph Lateral Scler       Date:  2010

Review 4.  The distal hereditary motor neuropathies.

Authors:  Alexander M Rossor; Bernadett Kalmar; Linda Greensmith; Mary M Reilly
Journal:  J Neurol Neurosurg Psychiatry       Date:  2011-10-25       Impact factor: 10.154

5.  Structural and Mechanistic Regulation of the Pro-degenerative NAD Hydrolase SARM1.

Authors:  Matthew Bratkowski; Tian Xie; Desiree A Thayer; Shradha Lad; Prakhyat Mathur; Yu-San Yang; Gregory Danko; Thomas C Burdett; Jean Danao; Aaron Cantor; Jennifer A Kozak; Sean P Brown; Xiaochen Bai; Shilpa Sambashivan
Journal:  Cell Rep       Date:  2020-08-04       Impact factor: 9.423

6.  dSarm/Sarm1 is required for activation of an injury-induced axon death pathway.

Authors:  Jeannette M Osterloh; Jing Yang; Timothy M Rooney; A Nicole Fox; Robert Adalbert; Eric H Powell; Amy E Sheehan; Michelle A Avery; Rachel Hackett; Mary A Logan; Jennifer M MacDonald; Jennifer S Ziegenfuss; Stefan Milde; Ying-Ju Hou; Carl Nathan; Aihao Ding; Robert H Brown; Laura Conforti; Michael Coleman; Marc Tessier-Lavigne; Stephan Züchner; Marc R Freeman
Journal:  Science       Date:  2012-06-07       Impact factor: 47.728

7.  The NAD+-mediated self-inhibition mechanism of pro-neurodegenerative SARM1.

Authors:  Yuefeng Jiang; Tingting Liu; Chia-Hsueh Lee; Qing Chang; Jing Yang; Zhe Zhang
Journal:  Nature       Date:  2020-10-14       Impact factor: 49.962

8.  Sarm1, a negative regulator of innate immunity, interacts with syndecan-2 and regulates neuronal morphology.

Authors:  Chiung-Ya Chen; Chia-Wen Lin; Chiung-Ying Chang; Si-Tse Jiang; Yi-Ping Hsueh
Journal:  J Cell Biol       Date:  2011-05-09       Impact factor: 10.539

9.  A rise in NAD precursor nicotinamide mononucleotide (NMN) after injury promotes axon degeneration.

Authors:  M Di Stefano; I Nascimento-Ferreira; G Orsomando; V Mori; J Gilley; R Brown; L Janeckova; M E Vargas; L A Worrell; A Loreto; J Tickle; J Patrick; J R M Webster; M Marangoni; F M Carpi; S Pucciarelli; F Rossi; W Meng; A Sagasti; R R Ribchester; G Magni; M P Coleman; L Conforti
Journal:  Cell Death Differ       Date:  2014-10-17       Impact factor: 15.828

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  12 in total

1.  Selective inhibitors of SARM1 targeting an allosteric cysteine in the autoregulatory ARM domain.

Authors:  Hannah C Feldman; Elisa Merlini; Carlos Guijas; Kristen E DeMeester; Evert Njomen; Ellen M Kozina; Minoru Yokoyama; Ekaterina Vinogradova; Holly T Reardon; Bruno Melillo; Stuart L Schreiber; Andrea Loreto; Jacqueline L Blankman; Benjamin F Cravatt
Journal:  Proc Natl Acad Sci U S A       Date:  2022-08-22       Impact factor: 12.779

Review 2.  Axon Biology in ALS: Mechanisms of Axon Degeneration and Prospects for Therapy.

Authors:  Michael P Coleman
Journal:  Neurotherapeutics       Date:  2022-10-07       Impact factor: 6.088

3.  Distinct developmental and degenerative functions of SARM1 require NAD+ hydrolase activity.

Authors:  E J Brace; Kow Essuman; Xianrong Mao; John Palucki; Yo Sasaki; Jeff Milbrandt; Aaron DiAntonio
Journal:  PLoS Genet       Date:  2022-06-23       Impact factor: 6.020

Review 4.  DNA Damage, Defective DNA Repair, and Neurodegeneration in Amyotrophic Lateral Sclerosis.

Authors:  Anna Konopka; Julie D Atkin
Journal:  Front Aging Neurosci       Date:  2022-04-27       Impact factor: 5.702

5.  Constitutively active SARM1 variants that induce neuropathy are enriched in ALS patients.

Authors:  A Joseph Bloom; Xianrong Mao; Amy Strickland; Yo Sasaki; Jeffrey Milbrandt; Aaron DiAntonio
Journal:  Mol Neurodegener       Date:  2022-01-06       Impact factor: 14.195

Review 6.  Lessons from Injury: How Nerve Injury Studies Reveal Basic Biological Mechanisms and Therapeutic Opportunities for Peripheral Nerve Diseases.

Authors:  Peter Arthur-Farraj; Michael P Coleman
Journal:  Neurotherapeutics       Date:  2021-09-30       Impact factor: 7.620

7.  SARM1 is a multi-functional NAD(P)ase with prominent base exchange activity, all regulated bymultiple physiologically relevant NAD metabolites.

Authors:  Carlo Angeletti; Adolfo Amici; Jonathan Gilley; Andrea Loreto; Antonio G Trapanotto; Christina Antoniou; Elisa Merlini; Michael P Coleman; Giuseppe Orsomando
Journal:  iScience       Date:  2022-01-25

Review 8.  NAD+ Metabolism and Diseases with Motor Dysfunction.

Authors:  Samuel Lundt; Shinghua Ding
Journal:  Genes (Basel)       Date:  2021-11-09       Impact factor: 4.096

9.  Sarm1 haploinsufficiency or low expression levels after antisense oligonucleotides delay programmed axon degeneration.

Authors:  Stacey Anne Gould; Jonathan Gilley; Karen Ling; Paymaan Jafar-Nejad; Frank Rigo; Michael Coleman
Journal:  Cell Rep       Date:  2021-12-14       Impact factor: 9.423

10.  Neurotoxin-mediated potent activation of the axon degeneration regulator SARM1.

Authors:  Andrea Loreto; Carlo Angeletti; Giuseppe Orsomando; Michael P Coleman; Weixi Gu; Andrew Osborne; Bart Nieuwenhuis; Jonathan Gilley; Elisa Merlini; Peter Arthur-Farraj; Adolfo Amici; Zhenyao Luo; Lauren Hartley-Tassell; Thomas Ve; Laura M Desrochers; Qi Wang; Bostjan Kobe
Journal:  Elife       Date:  2021-12-06       Impact factor: 8.713

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