RNA methyltransferase SPOUT1/CENP-32 links mitotic spindle organization with the neurodevelopmental disorder SpADMiSS

A Avinash V. Dharmadhikari M Maria Alba Abad S Sheraz Khan R Reza Maroofian T Tristan T. Sands F Farid Ullah I Itaru Samejima Y Yanwen Shen M Martin A. Wear K Kiara E. Moore E Elena Kondakova N Natalia Mitina T Theres Schaub G Grace K. Lee C Christine H. Umandap S Sara M. Berger A Alejandro D. Iglesias B Bernt Popp R Rami Abou Jamra H Heinz Gabriel S Stefan Rentas A Alyssa L. Rippert C Christopher Gray K Kosuke Izumi L Laura K. Conlin D Daniel C. Koboldt T Theresa Mihalic Mosher S Scott E. Hickey D Dara V. F. Albert H Haley Norwood A Amy Feldman Lewanda H Hongzheng Dai P Pengfei Liu T Tadahiro Mitani D Dana Marafi H Hatice Koçak Eker D Davut Pehlivan J Jennifer E. Posey N Natalie C. Lippa N Natalie Vena E Erin L. Heinzen D David B. Goldstein C Cyril Mignot (Département de Génétique, Groupe Hospitalier Pitié-Salpêtrière and Hôpital Trousseau and Centre de Référence Maladies Rares Déficiences Intellectuelles de Causes Rares, Assistance Publique-Hopitaux de Paris Sorbonne Université) J Jean-Madeleine de Sainte Agathe N Nouriya Abbas Al-Sannaa M Mina Zamani S Saeid Sadeghian R Reza Azizimalamiri T Tahere Seifia M Maha S. Zaki G Ghada M. H. Abdel-Salam M Mohamed S. Abdel-Hamid L Lama AlAbdi F Fowzan Sami Alkuraya H Heba Dawoud A Aya Lofty P Peter Bauer G Giovanni Zifarelli E Erum Afzal F Faisal Zafar S Stephanie Efthymiou D Daniel Gossett M Meghan C. Towne R Raey Yeneabat B Belen Perez-Duenas A Ana Cazurro-Gutierrez E Edgard Verdura V Veronica Cantarin-Extremera A Ana do Vale Marques A Aleksandra Helwak D David Tollervey S Sandeep N. Wontakal V Vimla S. Aggarwal J Jill A. Rosenfeld V Victor Tarabykin S Shinya Ohta J James R. Lupski H Henry Houlden W William C. Earnshaw E Erica E. Davis A A. Arockia Jeyaprakash J Jun Liao (Institute of Systems Biomedicine, School of Basic Medical Sciences)

Abstract

Abstract SPOUT1/CENP-32 encodes a putative SPOUT RNA methyltransferase previously identified as a mitotic chromosome associated protein. SPOUT1/CENP-32 depletion leads to centrosome detachment from the spindle poles and chromosome misalignment. Aided by gene matching platforms, here we identify 28 individuals with neurodevelopmental delays from 21 families with bi-allelic variants in SPOUT1/CENP-32 detected by exome/genome sequencing. Zebrafish spout1/cenp-32 mutants show reduction in larval head size with concomitant apoptosis likely associated with altered cell cycle progression. In vivo complementation assays in zebrafish indicate that SPOUT1/CENP-32 missense variants identified in humans are pathogenic. Crystal structure analysis of SPOUT1/CENP-32 reveals that most disease-associated missense variants are located within the catalytic domain. Additionally, SPOUT1/CENP-32 recurrent missense variants show reduced methyltransferase activity in vitro and compromised centrosome tethering to the spindle poles in human cells. Thus, SPOUT1/CENP-32 pathogenic variants cause an autosomal recessive neurodevelopmental disorder: SpADMiSS ( SPOUT1 Associated Development delay Microcephaly Seizures Short stature) underpinned by mitotic spindle organization defects and consequent chromosome segregation errors.

Article Details

Volume / Issue Vol. 16, Issue 1
Published February 17, 2025
ISSN 2041-1723
Publisher Nature Portfolio

Journal Info

Nature Communications

Nature Portfolio

ISSN: 2041-1723 Open Access Life Sciences

Authors (82)

A

Avinash V. Dharmadhikari

M

Maria Alba Abad

S

Sheraz Khan

R

Reza Maroofian

T

Tristan T. Sands

F

Farid Ullah

I

Itaru Samejima

Y

Yanwen Shen

M

Martin A. Wear

K

Kiara E. Moore

E

Elena Kondakova

N

Natalia Mitina

T

Theres Schaub

G

Grace K. Lee

C

Christine H. Umandap

S

Sara M. Berger

A

Alejandro D. Iglesias

B

Bernt Popp

R

Rami Abou Jamra

H

Heinz Gabriel

S

Stefan Rentas

A

Alyssa L. Rippert

C

Christopher Gray

K

Kosuke Izumi

L

Laura K. Conlin

D

Daniel C. Koboldt

T

Theresa Mihalic Mosher

S

Scott E. Hickey

D

Dara V. F. Albert

H

Haley Norwood

A

Amy Feldman Lewanda

H

Hongzheng Dai

P

Pengfei Liu

T

Tadahiro Mitani

D

Dana Marafi

H

Hatice Koçak Eker

D

Davut Pehlivan

J

Jennifer E. Posey

N

Natalie C. Lippa

N

Natalie Vena

E

Erin L. Heinzen

D

David B. Goldstein

C

Cyril Mignot

Département de Génétique, Groupe Hospitalier Pitié-Salpêtrière and Hôpital Trousseau and Centre de Référence Maladies Rares Déficiences Intellectuelles de Causes Rares, Assistance Publique-Hopitaux de Paris Sorbonne Université

J

Jean-Madeleine de Sainte Agathe

N

Nouriya Abbas Al-Sannaa

M

Mina Zamani

S

Saeid Sadeghian

R

Reza Azizimalamiri

T

Tahere Seifia

M

Maha S. Zaki

G

Ghada M. H. Abdel-Salam

M

Mohamed S. Abdel-Hamid

L

Lama AlAbdi

F

Fowzan Sami Alkuraya

H

Heba Dawoud

A

Aya Lofty

P

Peter Bauer

G

Giovanni Zifarelli

E

Erum Afzal

F

Faisal Zafar

S

Stephanie Efthymiou

D

Daniel Gossett

M

Meghan C. Towne

R

Raey Yeneabat

B

Belen Perez-Duenas

A

Ana Cazurro-Gutierrez

E

Edgard Verdura

V

Veronica Cantarin-Extremera

A

Ana do Vale Marques

A

Aleksandra Helwak

D

David Tollervey

S

Sandeep N. Wontakal

V

Vimla S. Aggarwal

J

Jill A. Rosenfeld

V

Victor Tarabykin

S

Shinya Ohta

J

James R. Lupski

H

Henry Houlden

W

William C. Earnshaw

E

Erica E. Davis

A

A. Arockia Jeyaprakash

J

Jun Liao

Institute of Systems Biomedicine, School of Basic Medical Sciences