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ATMIN is a transcriptional regulator of both lung morphogenesis and ciliogenesis

ATMIN is a transcriptional regulator of both lung morphogenesis and ciliogenesis
ATMIN is a transcriptional regulator of both lung morphogenesis and ciliogenesis
Initially identified in DNA damage repair, ATM-interactor (ATMIN) further functions as a transcriptional regulator of lung morphogenesis. Here we analyse three mouse mutants, Atmin(gpg6/gpg6), Atmin(H210Q/H210Q) and Dynll1(GT/GT), revealing how ATMIN and its transcriptional target dynein light chain LC8-type 1 (DYNLL1) are required for normal lung morphogenesis and ciliogenesis. Expression screening of ciliogenic genes confirmed Dynll1 to be controlled by ATMIN and further revealed moderately altered expression of known intraflagellar transport (IFT) protein-encoding loci in Atmin mutant embryos. Significantly, Dynll1(GT/GT) embryonic cilia exhibited shortening and bulging, highly similar to the characterised retrograde IFT phenotype of Dync2h1. Depletion of ATMIN or DYNLL1 in cultured cells recapitulated the in vivo ciliogenesis phenotypes and expression of DYNLL1 or the related DYNLL2 rescued the effects of loss of ATMIN, demonstrating that ATMIN primarily promotes ciliogenesis by regulating Dynll1 expression. Furthermore, DYNLL1 as well as DYNLL2 localised to cilia in puncta, consistent with IFT particles, and physically interacted with WDR34, a mammalian homologue of the Chlamydomonas cytoplasmic dynein 2 intermediate chain that also localised to the cilium. This study extends the established Atmin-Dynll1 relationship into a developmental and a ciliary context, uncovering a novel series of interactions between DYNLL1, WDR34 and ATMIN. This identifies potential novel components of cytoplasmic dynein 2 and furthermore provides fresh insights into the molecular pathogenesis of human skeletal ciliopathies.
1477-9129
3966-3977
Goggolidou, P.
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Stevens, J.L.
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Agueci, F.
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Keynton, J.
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Wheway, G.
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Grimes, D.T.
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Patel, S.H.
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Hilton, H.
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Morthorst, S.K.
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DiPaolo, A.
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Williams, D.J.
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Sanderson, J.
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Khoronenkova, S.V.
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Powles-Glover, N.
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Ermakov, A.
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Esapa, C.T.
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Romero, R.
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Dianov, G.L.
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Briscoe, J.
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Johnson, C.A.
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Pedersen, L.B.
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Norris, D.P.
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Goggolidou, P.
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Stevens, J.L.
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Agueci, F.
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Keynton, J.
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Wheway, G.
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Grimes, D.T.
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Patel, S.H.
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Hilton, H.
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Morthorst, S.K.
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DiPaolo, A.
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Williams, D.J.
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Sanderson, J.
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Khoronenkova, S.V.
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Powles-Glover, N.
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Ermakov, A.
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Esapa, C.T.
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Romero, R.
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Dianov, G.L.
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Briscoe, J.
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Johnson, C.A.
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Pedersen, L.B.
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Norris, D.P.
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Goggolidou, P., Stevens, J.L., Agueci, F., Keynton, J., Wheway, G., Grimes, D.T., Patel, S.H., Hilton, H., Morthorst, S.K., DiPaolo, A., Williams, D.J., Sanderson, J., Khoronenkova, S.V., Powles-Glover, N., Ermakov, A., Esapa, C.T., Romero, R., Dianov, G.L., Briscoe, J., Johnson, C.A., Pedersen, L.B. and Norris, D.P. (2014) ATMIN is a transcriptional regulator of both lung morphogenesis and ciliogenesis. Development, 141 (20), 3966-3977. (doi:10.1242/dev.107755).

Record type: Article

Abstract

Initially identified in DNA damage repair, ATM-interactor (ATMIN) further functions as a transcriptional regulator of lung morphogenesis. Here we analyse three mouse mutants, Atmin(gpg6/gpg6), Atmin(H210Q/H210Q) and Dynll1(GT/GT), revealing how ATMIN and its transcriptional target dynein light chain LC8-type 1 (DYNLL1) are required for normal lung morphogenesis and ciliogenesis. Expression screening of ciliogenic genes confirmed Dynll1 to be controlled by ATMIN and further revealed moderately altered expression of known intraflagellar transport (IFT) protein-encoding loci in Atmin mutant embryos. Significantly, Dynll1(GT/GT) embryonic cilia exhibited shortening and bulging, highly similar to the characterised retrograde IFT phenotype of Dync2h1. Depletion of ATMIN or DYNLL1 in cultured cells recapitulated the in vivo ciliogenesis phenotypes and expression of DYNLL1 or the related DYNLL2 rescued the effects of loss of ATMIN, demonstrating that ATMIN primarily promotes ciliogenesis by regulating Dynll1 expression. Furthermore, DYNLL1 as well as DYNLL2 localised to cilia in puncta, consistent with IFT particles, and physically interacted with WDR34, a mammalian homologue of the Chlamydomonas cytoplasmic dynein 2 intermediate chain that also localised to the cilium. This study extends the established Atmin-Dynll1 relationship into a developmental and a ciliary context, uncovering a novel series of interactions between DYNLL1, WDR34 and ATMIN. This identifies potential novel components of cytoplasmic dynein 2 and furthermore provides fresh insights into the molecular pathogenesis of human skeletal ciliopathies.

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Accepted/In Press date: 20 August 2014
e-pub ahead of print date: 7 October 2014
Published date: October 2014

Identifiers

Local EPrints ID: 423514
URI: http://eprints.soton.ac.uk/id/eprint/423514
ISSN: 1477-9129
PURE UUID: cd0bd303-e41b-438b-b192-4cb335e631e8
ORCID for G. Wheway: ORCID iD orcid.org/0000-0002-0494-0783

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Date deposited: 25 Sep 2018 16:30
Last modified: 16 Mar 2024 04:38

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Contributors

Author: P. Goggolidou
Author: J.L. Stevens
Author: F. Agueci
Author: J. Keynton
Author: G. Wheway ORCID iD
Author: D.T. Grimes
Author: S.H. Patel
Author: H. Hilton
Author: S.K. Morthorst
Author: A. DiPaolo
Author: D.J. Williams
Author: J. Sanderson
Author: S.V. Khoronenkova
Author: N. Powles-Glover
Author: A. Ermakov
Author: C.T. Esapa
Author: R. Romero
Author: G.L. Dianov
Author: J. Briscoe
Author: C.A. Johnson
Author: L.B. Pedersen
Author: D.P. Norris

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