ATR promotes cilia signalling: links to developmental impacts

Hum Mol Genet. 2016 Apr 15;25(8):1574-87. doi: 10.1093/hmg/ddw034. Epub 2016 Feb 11.

Abstract

Mutations in ATR(ataxia telangiectasia and RAD3-related) cause Seckel syndrome (ATR-SS), a microcephalic primordial dwarfism disorder. Hitherto, the clinical manifestation of ATR deficiency has been attributed to its canonical role in DNA damage response signalling following replication fork stalling/collapse. Here, we show that ATR regulates cilia-dependent signalling in a manner that can be uncoupled from its function during replication. ATR-depleted or patient-derived ATR-SS cells form cilia of slightly reduced length but are dramatically impaired in cilia-dependent signalling functions, including growth factor and Sonic hedgehog signalling. To better understand the developmental impact of ATR loss of function, we also used zebrafish as a model. Zebrafish embryos depleted of Atr resembled ATR-SS morphology, showed a modest but statistically significant reduction in cilia length and other morphological features indicative of cilia dysfunction. Additionally, they displayed defects in left-right asymmetry including ambiguous expression of southpaw, incorrectly looped hearts and randomized localization of internal organs including the pancreas, features typically conferred by cilia dysfunction. Our findings reveal a novel role for ATR in cilia signalling distinct from its canonical function during replication and strengthen emerging links between cilia function and development.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Ataxia Telangiectasia Mutated Proteins / genetics
  • Ataxia Telangiectasia Mutated Proteins / metabolism*
  • Cell Line
  • Cilia / metabolism
  • Cilia / pathology*
  • DNA Replication
  • Disease Models, Animal
  • Dwarfism / genetics
  • Dwarfism / pathology*
  • Facies
  • Gene Expression Regulation, Developmental
  • Humans
  • Microcephaly / genetics
  • Microcephaly / pathology*
  • Signal Transduction
  • Zebrafish / embryology*
  • Zebrafish / genetics
  • Zebrafish / metabolism
  • Zebrafish Proteins / genetics
  • Zebrafish Proteins / metabolism*

Substances

  • Zebrafish Proteins
  • ATR protein, human
  • ATR protein, zebrafish
  • Ataxia Telangiectasia Mutated Proteins

Supplementary concepts

  • Seckel syndrome 1