The ciliopathy-associated CPLANE proteins direct basal body recruitment of intraflagellar transport machinery

Michinori Toriyama; Chanjae Lee; S. Paige Taylor; Ivan Duran; Daniel H. Cohn; Ange Line Bruel; Jacqueline M. Tabler; Kevin Drew; Marcus R. Kelly; Sukyoung Kim; Tae Joo Park; Daniella Braun; Ghislaine Pierquin; Armand Biver; Kerstin Wagner; Anne Malfroot; Inusha Panigrahi; Brunella Franco; Hadeel Adel Al-lami; Yvonne Yeung; Yeon Ja Choi; Yannis Duffourd; Laurence Faivre; Jean Baptiste Rivière; Jiang Chen; Karen J. Liu; Edward M. Marcotte; Friedhelm Hildebrandt; Christel Thauvin-Robinet; Deborah Krakow; Peter K. Jackson; John B. Wallingford

doi:10.1038/ng.3558

The ciliopathy-associated CPLANE proteins direct basal body recruitment of intraflagellar transport machinery

Michinori Toriyama, Chanjae Lee, S. Paige Taylor, Ivan Duran, Daniel H. Cohn, Ange Line Bruel, Jacqueline M. Tabler, Kevin Drew, Marcus R. Kelly, Sukyoung Kim, Tae Joo Park, Daniella Braun, Ghislaine Pierquin, Armand Biver, Kerstin Wagner, Anne Malfroot, Inusha Panigrahi, Brunella Franco, Hadeel Adel Al-lami, Yvonne YeungYeon Ja Choi, Yannis Duffourd, Laurence Faivre, Jean Baptiste Rivière, Jiang Chen, Karen J. Liu, Edward M. Marcotte, Friedhelm Hildebrandt, Christel Thauvin-Robinet, Deborah Krakow, Peter K. Jackson, John B. Wallingford^*

^*Corresponding author for this work

Centre for Craniofacial & Regenerative Biology

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

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Abstract

Cilia use microtubule-based intraflagellar transport (IFT) to organize intercellular signaling. Ciliopathies are a spectrum of human diseases resulting from defects in cilia structure or function. The mechanisms regulating the assembly of ciliary multiprotein complexes and the transport of these complexes to the base of cilia remain largely unknown. Combining proteomics, in vivo imaging and genetic analysis of proteins linked to planar cell polarity (Inturned, Fuzzy and Wdpcp), we identified and characterized a new genetic module, which we term CPLANE (ciliogenesis and planar polarity effector), and an extensive associated protein network. CPLANE proteins physically and functionally interact with the poorly understood ciliopathy-associated protein Jbts17 at basal bodies, where they act to recruit a specific subset of IFT-A proteins. In the absence of CPLANE, defective IFT-A particles enter the axoneme and IFT-B trafficking is severely perturbed. Accordingly, mutation of CPLANE genes elicits specific ciliopathy phenotypes in mouse models and is associated with ciliopathies in human patients.

Original language	English
Pages (from-to)	648-656
Number of pages	9
Journal	Nature Genetics
Volume	48
Issue number	6
Early online date	9 May 2016
DOIs	https://doi.org/10.1038/ng.3558
Publication status	Published - 1 Jun 2016

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The ciliopathy-associated_TORIYAMA_Accepted1April2016_GREEN AAMAccepted author manuscript, 1.91 MB

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Toriyama, M., Lee, C., Taylor, S. P., Duran, I., Cohn, D. H., Bruel, A. L., Tabler, J. M., Drew, K., Kelly, M. R., Kim, S., Park, T. J., Braun, D., Pierquin, G., Biver, A., Wagner, K., Malfroot, A., Panigrahi, I., Franco, B., Al-lami, H. A., ... Wallingford, J. B. (2016). The ciliopathy-associated CPLANE proteins direct basal body recruitment of intraflagellar transport machinery. Nature Genetics, 48(6), 648-656. https://doi.org/10.1038/ng.3558

@article{25609eb6780c46c9a4e74ca2a8827ea1,

title = "The ciliopathy-associated CPLANE proteins direct basal body recruitment of intraflagellar transport machinery",

abstract = "Cilia use microtubule-based intraflagellar transport (IFT) to organize intercellular signaling. Ciliopathies are a spectrum of human diseases resulting from defects in cilia structure or function. The mechanisms regulating the assembly of ciliary multiprotein complexes and the transport of these complexes to the base of cilia remain largely unknown. Combining proteomics, in vivo imaging and genetic analysis of proteins linked to planar cell polarity (Inturned, Fuzzy and Wdpcp), we identified and characterized a new genetic module, which we term CPLANE (ciliogenesis and planar polarity effector), and an extensive associated protein network. CPLANE proteins physically and functionally interact with the poorly understood ciliopathy-associated protein Jbts17 at basal bodies, where they act to recruit a specific subset of IFT-A proteins. In the absence of CPLANE, defective IFT-A particles enter the axoneme and IFT-B trafficking is severely perturbed. Accordingly, mutation of CPLANE genes elicits specific ciliopathy phenotypes in mouse models and is associated with ciliopathies in human patients.",

author = "Michinori Toriyama and Chanjae Lee and Taylor, {S. Paige} and Ivan Duran and Cohn, {Daniel H.} and Bruel, {Ange Line} and Tabler, {Jacqueline M.} and Kevin Drew and Kelly, {Marcus R.} and Sukyoung Kim and Park, {Tae Joo} and Daniella Braun and Ghislaine Pierquin and Armand Biver and Kerstin Wagner and Anne Malfroot and Inusha Panigrahi and Brunella Franco and Al-lami, {Hadeel Adel} and Yvonne Yeung and Choi, {Yeon Ja} and Yannis Duffourd and Laurence Faivre and Rivi{\`e}re, {Jean Baptiste} and Jiang Chen and Liu, {Karen J.} and Marcotte, {Edward M.} and Friedhelm Hildebrandt and Christel Thauvin-Robinet and Deborah Krakow and Jackson, {Peter K.} and Wallingford, {John B.}",

year = "2016",

month = jun,

day = "1",

doi = "10.1038/ng.3558",

language = "English",

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Toriyama, M, Lee, C, Taylor, SP, Duran, I, Cohn, DH, Bruel, AL, Tabler, JM, Drew, K, Kelly, MR, Kim, S, Park, TJ, Braun, D, Pierquin, G, Biver, A, Wagner, K, Malfroot, A, Panigrahi, I, Franco, B, Al-lami, HA, Yeung, Y, Choi, YJ, Duffourd, Y, Faivre, L, Rivière, JB, Chen, J, Liu, KJ, Marcotte, EM, Hildebrandt, F, Thauvin-Robinet, C, Krakow, D, Jackson, PK & Wallingford, JB 2016, 'The ciliopathy-associated CPLANE proteins direct basal body recruitment of intraflagellar transport machinery', Nature Genetics, vol. 48, no. 6, pp. 648-656. https://doi.org/10.1038/ng.3558

TY - JOUR

T1 - The ciliopathy-associated CPLANE proteins direct basal body recruitment of intraflagellar transport machinery

AU - Toriyama, Michinori

AU - Lee, Chanjae

AU - Taylor, S. Paige

AU - Duran, Ivan

AU - Cohn, Daniel H.

AU - Bruel, Ange Line

AU - Tabler, Jacqueline M.

AU - Drew, Kevin

AU - Kelly, Marcus R.

AU - Kim, Sukyoung

AU - Park, Tae Joo

AU - Braun, Daniella

AU - Pierquin, Ghislaine

AU - Biver, Armand

AU - Wagner, Kerstin

AU - Malfroot, Anne

AU - Panigrahi, Inusha

AU - Franco, Brunella

AU - Al-lami, Hadeel Adel

AU - Yeung, Yvonne

AU - Choi, Yeon Ja

AU - Duffourd, Yannis

AU - Faivre, Laurence

AU - Rivière, Jean Baptiste

AU - Chen, Jiang

AU - Liu, Karen J.

AU - Marcotte, Edward M.

AU - Hildebrandt, Friedhelm

AU - Thauvin-Robinet, Christel

AU - Krakow, Deborah

AU - Jackson, Peter K.

AU - Wallingford, John B.

PY - 2016/6/1

Y1 - 2016/6/1

N2 - Cilia use microtubule-based intraflagellar transport (IFT) to organize intercellular signaling. Ciliopathies are a spectrum of human diseases resulting from defects in cilia structure or function. The mechanisms regulating the assembly of ciliary multiprotein complexes and the transport of these complexes to the base of cilia remain largely unknown. Combining proteomics, in vivo imaging and genetic analysis of proteins linked to planar cell polarity (Inturned, Fuzzy and Wdpcp), we identified and characterized a new genetic module, which we term CPLANE (ciliogenesis and planar polarity effector), and an extensive associated protein network. CPLANE proteins physically and functionally interact with the poorly understood ciliopathy-associated protein Jbts17 at basal bodies, where they act to recruit a specific subset of IFT-A proteins. In the absence of CPLANE, defective IFT-A particles enter the axoneme and IFT-B trafficking is severely perturbed. Accordingly, mutation of CPLANE genes elicits specific ciliopathy phenotypes in mouse models and is associated with ciliopathies in human patients.

AB - Cilia use microtubule-based intraflagellar transport (IFT) to organize intercellular signaling. Ciliopathies are a spectrum of human diseases resulting from defects in cilia structure or function. The mechanisms regulating the assembly of ciliary multiprotein complexes and the transport of these complexes to the base of cilia remain largely unknown. Combining proteomics, in vivo imaging and genetic analysis of proteins linked to planar cell polarity (Inturned, Fuzzy and Wdpcp), we identified and characterized a new genetic module, which we term CPLANE (ciliogenesis and planar polarity effector), and an extensive associated protein network. CPLANE proteins physically and functionally interact with the poorly understood ciliopathy-associated protein Jbts17 at basal bodies, where they act to recruit a specific subset of IFT-A proteins. In the absence of CPLANE, defective IFT-A particles enter the axoneme and IFT-B trafficking is severely perturbed. Accordingly, mutation of CPLANE genes elicits specific ciliopathy phenotypes in mouse models and is associated with ciliopathies in human patients.

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U2 - 10.1038/ng.3558

DO - 10.1038/ng.3558

M3 - Article

AN - SCOPUS:84966600215

SN - 1061-4036

VL - 48

SP - 648

EP - 656

JO - Nature Genetics

JF - Nature Genetics

IS - 6

ER -

The ciliopathy-associated CPLANE proteins direct basal body recruitment of intraflagellar transport machinery

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