Evolutionary Proteomics Uncovers Ancient Associations of Cilia with Signaling Pathways

Sigg, Monika Abedin; Menchen, Tabea; Lee, Chanjae; Johnson, Jeffery; Jungnickel, Melissa K.; Choksi, Semil P.; Garcia, Galo; Busengdal, Henriette; Dougherty, Gerard W.; Pennekamp, Petra; Werner, Claudius; Rentzsch, Fabian; Florman, Harvey M.; Krogan, Nevan; Wallingford, John B.; Omran, Heymut; Reiter, Jeremy F.

doi:10.1016/j.devcel.2017.11.014

Cited by 130Genetic and Kidney Cyst DiseasesCystic Fibrosis Research AdvancesHedgehog Signaling Pathway Studies

Evolutionary Proteomics Uncovers Ancient Associations of Cilia with Signaling Pathways

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Sigg, Monika Abedin, Menchen, Tabea, Lee, Chanjae, Johnson, Jeffery, Jungnickel, Melissa K., Choksi, Semil P., Garcia, Galo, Busengdal, Henriette +9 more·2017·Developmental Cell

DOI 10.1016/j.devcel.2017.11.014PMC PMC5752135

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Abstract

Cilia are organelles specialized for movement and signaling. To infer when during evolution signaling pathways became associated with cilia, we characterized the proteomes of cilia from sea urchins, sea anemones, and choanoflagellates. We identified 437 high-confidence ciliary candidate proteins conserved in mammals and discovered that Hedgehog and G-protein-coupled receptor pathways were linked to cilia before the origin of bilateria and transient receptor potential (TRP) channels before the origin of animals. We demonstrated that candidates not previously implicated in ciliary biology localized to cilia and further investigated ENKUR, a TRP channel-interacting protein identified in the cilia of all three organisms. ENKUR localizes to motile cilia and is required for patterning the left-right axis in vertebrates. Moreover, mutation of ENKUR causes situs inversus in humans. Thus, proteomic profiling of cilia from diverse eukaryotes defines a conserved ciliary proteome, reveals ancient connections to signaling, and uncovers a ciliary protein that underlies development and human disease.

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Enkurin (CFAP106) localises near the inner junction and its disruption leads to situs inversus in humans.
“Another protein, Enkurin (CFAP106) also localises near the inner junction and its disruption similarly leads to situs inversus in humans81, with ciliary motility defects also as a potential aetiology82.”
From The inner junction protein CFAP20 functions in motile and non-motile cilia and is critical for vision (2022) · cites this paper as [81]
In Results, under “Mutation of human ENKUR affects left-right axis specification” (page not supplied), the paper reports two people with situs inversus totalis whose homozygous ENKUR variant co-segregated with the condition; it says the findings suggest ENKUR mutations are a cause. It also locates ENKUR in human nasal cilia, but does not place it near the inner junction. The claim therefore adds an unsupported location and states the human causal link more firmly than the paper does. (LLM, conf=0.87)
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Omran H Kobayashi D Olbrich H Tsukahara T Loges NT Hagiwara H Zhang Q Leblond G O’Toole E Hara C 2008b Ktu/PF13 is required for cytoplasmic pre-assembly of axonemal dyneins Nature 456 611 616 19052621 PMC3279746

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ARL13B regulates Sonic hedgehog signaling from outside primary cilia
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Sperm Differentiation: The Role of Trafficking of Proteins
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Seriously cilia: A tiny organelle illuminates evolution, disease, and intercellular communication
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The hedgehog pathway and ocular developmental anomalies
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The transcriptional signature associated with human motile cilia
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The essential role of primary cilia in cerebral cortical development and disorders
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Identification of eQTLs and sQTLs associated with meat quality in beef
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Motile cilia genetics and cell biology: big results from little mice
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Intrinsic heterogeneity of primary cilia revealed through spatial proteomics
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Cilia and development
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The neuronal cilium – a highly diverse and dynamic organelle involved in sensory detection and neuromodulation
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Centrosomal and ciliary targeting of CCDC66 requires cooperative action of centriolar satellites, microtubules and molecular motors
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Exploring the Uncharacterized Human Proteome Using neXtProt
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Primary Cilia and Calcium Signaling Interactions
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E3 ubiquitin ligase Wwp1 regulates ciliary dynamics of the Hedgehog receptor Smoothened
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Primary Ciliary Dyskinesia
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FAP57/WDR65 targets assembly of a subset of inner arm dyneins and connects to regulatory hubs in cilia
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Androglobin gene expression patterns and FOXJ1-dependent regulation indicate its functional association with ciliogenesis
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What is it like to be a choanoflagellate? Sensation, processing and behavior in the closest unicellular relatives of animals
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Composition of Caenorhabditis elegans extracellular vesicles suggests roles in metabolism, immunity, and aging
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The deubiquitinating enzyme Usp14 controls ciliogenesis and Hedgehog signaling
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Androglobin, a chimeric mammalian globin, is required for male fertility
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Three-dimensional flagella structures from animals’ closest unicellular relatives, the Choanoflagellates
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The inner junction protein CFAP20 functions in motile and non-motile cilia and is critical for vision
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The mitochondrial transporter SLC25A25 links ciliary TRPP2 signaling and cellular metabolism
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A Proximity Mapping Journey into the Biology of the Mammalian Centrosome/Cilium Complex
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Nephronophthisis-Pathobiology and Molecular Pathogenesis of a Rare Kidney Genetic Disease
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CilioGenics: an integrated method and database for predicting novel ciliary genes
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Protein turnover dynamics suggest a diffusion-to-capture mechanism for peri-basal body recruitment and retention of intraflagellar transport proteins
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ENKD1 promotes epidermal stratification by regulating spindle orientation in basal keratinocytes
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ENKD1 promotes CP110 removal through competing with CEP97 to initiate ciliogenesis
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A phylogenetic profiling approach identifies novel ciliogenesis genes in Drosophila and C. elegans
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An RFX transcription factor regulates ciliogenesis in the closest living relatives of animals
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The flagellar protein Enkurin is required for mouse sperm motility and for transport through the female reproductive tract†
Jungnickel, M. K., Sutton, K. A., Baker, M. A., Cohen, M. G., Sanderson, M. J., & Florman, H. M. (2018) · Biology of Reproduction · doi:10.1093/biolre/ioy105 · Cited by 27 · see citing works
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The TRPP2-dependent channel of renal primary cilia also requires TRPM3
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Ciliary and cytoskeletal functions of an ancient monooxygenase essential for bioactive amidated peptide synthesis
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Sterol and oxysterol synthases near the ciliary base activate the Hedgehog pathway
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HTR6 and SSTR3 targeting to primary cilia
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Simple Method To Characterize the Ciliary Proteome of Multiciliated Cells
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Cell polarity in the protist-to-animal transition
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Gene Regulatory Network that Shaped the Evolution of Larval Apical Organ in Cnidaria
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Directional ciliary beats across epithelia require Ccdc57-mediated coupling between axonemal orientation and basal body polarity
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An amino acid-resolution interactome for motile cilia identifies the structure and function of ciliopathy protein complexes
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Ankrd45 Is a Novel Ankyrin Repeat Protein Required for Cell Proliferation
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WDR31 displays functional redundancy with GTPase-activating proteins (GAPs) ELMOD and RP2 in regulating IFT complex and recruiting the BBSome to cilium
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RETRACTED: ENKUR recruits FBXW7 to ubiquitinate and degrade MYH9 and further suppress MYH9‐induced deubiquitination of β‐catenin to block gastric cancer metastasis
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The conserved ancestral signaling pathway from cilium to nucleus
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ENKD1 is a centrosomal and ciliary microtubule‐associated protein important for primary cilium content regulation
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A temperature-induced sex reversal mechanism in ricefield eels
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Taxon-specific expansion and loss of tektins inform metazoan ciliary diversity
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Mechanical strain, novel genes and evolutionary insights: news from the frog left-right organizer
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Unraveling the intricate microtubule inner protein networks that reinforce mammalian sperm flagellaPreprint
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Contribution of Mass Spectrometry-Based Proteomics to Discoveries in Developmental Biology
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Microtubule inner proteins – bridging structure and function in ciliary biology
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Ordered deployment of distinct ciliary beating machines in growing axonemes of vertebrate multiciliated cells
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The evolutionary origins of synaptic proteins and their changing roles in different organisms across evolution
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Primary ciliary dyskinesia
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An Amino Acid-Resolution Interactome for Motile Cilia Illuminates the Structure and Function of Ciliopathy Protein ComplexesPreprint
McCafferty, C. L., Papoulas, O., Lee, C., Bui, K. H., Taylor, D. W., Marcotte, E. M., & Wallingford, J. B. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.07.09.548259 · Cited by 7 · see citing works
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Proximity labeling proteomics maps radial glial ciliary proteins across the developing telencephalon
Liu, X., Gutierrez, O. T., Baboo, S., Cai, E., Kaur, G., Al-Issa, Y., Diedrich, J. K., Yates, J. R., & Ge, X. (2026) · Cell Reports · doi:10.1016/j.celrep.2026.117355 · Cited by 9 · see citing works
The structure of basal body inner junctions from Tetrahymena revealed by electron cryo-tomography
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Sea urchin embryonic cilia
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A protein interactome for the last eukaryotic common ancestor illuminates the biochemical basis of modern genetic diseases
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Localisation and function of key axonemal microtubule inner proteins and dynein docking complex members reveal extensive diversity among vertebrate motile cilia
Lu, H., Twan, W. K., Ikawa, Y., Khare, V. P., Mukherjee, I., Schou, K. B., Chua, K. X., Aqasha, A., Chakrabarti, S., Hamada, H., et al. (2024) · Development · doi:10.1242/dev.202737 · Cited by 5 · see citing works
A stress-responsive p38 signaling axis in choanoflagellates
Rutaganira, F. U., Coyle, M. C., Nguyen, M. H. T., Hernandez, I., Scopton, A. P., Dar, A. C., & King, N. (2025) · RSC Chemical Biology · doi:10.1039/d4cb00122b · Cited by 5 · see citing works
The evolutionary foundations of transcriptional regulation in animals
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A high-resolution spatial map of cilia-associated proteins in the human fallopian tube
Hikmet, F., Digre, A., Hansen, J. N., Schon, S. B., Lundberg, E. K., Olovsson, M., Uhlén, M., Méar, L., & Lindskog, C. (2026) · Nature Communications · doi:10.1038/s41467-026-71692-6 · Cited by 5 · see citing works
Landmark contributions of Chlamydomonas to understanding cilia
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Purification and Analysis of Caenorhabditis elegans Extracellular Vesicles
Russell, J. C., Postupna, N. O., Golubeva, A., Keene, C. D., & Kaeberlein, M. R. (2020) · Journal of Visualized Experiments · doi:10.3791/60596 · Cited by 5 · see citing works
The inner junction complex of the cilia is an interaction hub that involves tubulin post-translational modificationsPreprint
Khalifa, A. A. Z., Ichikawa, M., Dai, D., Kubo, S., Black, C. S., Peri, K., McAlear, T. S., Veyron, S., Yang, S. K., Vargas, J., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/774695 · Cited by 5 · see citing works
The kinesin-4 protein KIF27 forms a cytoskeletal scaffold at the transition zone to promote motile cilia structural integrity
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Rare damaging variants in the sex differences of congenital heart disease: an exome sequencing study
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Biallelic Variants in MNS1 Are Associated with Laterality Defects and Respiratory Involvement
Hjeij, R., Leslie, J. S., Rizk, H., Dworniczak, B., Olbrich, H., Raidt, J., Bode, S. F. N., Gardham, A., Stals, K. L., Al-Haggar, M. S., et al. (2024) · Cells · doi:10.3390/cells13121017 · Cited by 4 · see citing works
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Molecular and cellular architecture of the larval sensory organ in the cnidarian Nematostella vectensisPreprint
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Proximity proteomics of primary cilia in human hypothalamic neuronsPreprint
Macarelli, V., Sroka, T. J., Hansen, J. N., Axelsson, U., Mick, D. U., & Merkle, F. T. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.05.11.653368 · Cited by 5 · see citing works
Is IIIG9 a New Protein with Exclusive Ciliary Function? Analysis of Its Potential Role in Cancer and Other Pathologies
Oviedo, M. J., Ramírez, E., Cifuentes, M., Farkas, C., Mella, A., Bertinat, R., Gajardo, R., Ferrada, L., Jara, N., Lima, I. D., et al. (2022) · Cells · doi:10.3390/cells11203327 · Cited by 2 · see citing works
Copy Number Variation Analysis of 5p Deletion Provides Accurate Prenatal Diagnosis and Reveals Candidate Pathogenic Genes
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Purification and Analysis of Caenorhabditis elegans Extracellular Vesicles
Russell, J. C., Postupna, N. O., Golubeva, A., Keene, C. D., & Kaeberlein, M. R. (2020) · Journal of Visualized Experiments · doi:10.3791/60596-v · Cited by 2 · see citing works
Gotta Go Slow: Two Evolutionarily Distinct Annelids Retain a Common Hedgehog Pathway Composition, Outlining Its Pan-Bilaterian Core
Platova, S. E., Poliushkevich, L. O., Kulakova, M. A., Nesterenko, M. A., Starunov, V. V., & Novikova, E. L. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms232214312 · Cited by 2 · see citing works
Primary Cilia
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Functional redundancy of WDR31 with GTPase-activating proteins ELMOD and RP2 in regulating IFT trains via BBSomePreprint
Cevik, S., Peng, X., Beyer, T., Pir, M. S., Yenisert, F., Woerz, F., Hoffmann, F., Altunkaynak, B., Pir, B., Boldt, K., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.06.10.445528 · Cited by 2 · see citing works
Proteomic profiling of primary cilia in the developing brain uncovers new regulators of cortical developmentPreprint
Liu, X., Gutierrez, O. T., Kaur, G., Al-Issa, Y., Baboo, S., Diedrich, J. K., Cai, E., Yates, J. R., & Ge, X. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.05.03.652041 · Cited by 2 · see citing works
Identification and bioinformatics analysis of cilia-associated gene families in Euplotes amieti (Ciliophora, Hypotrichia)
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Proximity labeling proteomics with cilia-TurboID transgenic mice identified regulators of motile cilia function
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Probing Cilia-Associated Signaling Proteomes in Animal Evolution
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Mechanical and chemical activation of GPR68 (OGR1) probed with a genetically-encoded fluorescent reporterPreprint
Ozkan, A. D., Gettas, T., Sogata, A., Phaychanpheng, W., & Lacroix, J. J. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.04.02.022251 · Cited by 1 · see citing works
WDR31 is a novel ciliopathy protein displaying functional redundancy with GTPase-activating proteins ELMOD and RP2 in recruiting BBSome to ciliumPreprint
Cevik, S., AlAbdi, L., Peng, X., Beyer, T., Zorluer, A., Pir, M. S., Yenisert, F., Shaheen, R., Woerz, F., Hoffmann, F., et al. (2021) · Research Square · doi:10.21203/rs.3.rs-622797/v1 · Cited by 1 · see citing works
Ciliopathies
Vogel, P., & Janke, L. J. (2021) · doi:10.1002/9781119624608.ch6 · Cited by 1 · see citing works

Probing Cilia-Associated Signaling Proteomes in Animal Evolution
Shulman, A., & Tsou, M.-F. B. (2017) · Developmental Cell · doi:10.1016/j.devcel.2017.12.009 · Cited by 1 · see citing works
The evolution of ciliary signaling mechanisms
Sigg, M. A., & Reiter, J. F. (2012) · Cilia · doi:10.1186/2046-2530-1-s1-p11
Self-citation
Letter Fast T rack Hedgehog Signaling Requires Motile Cilia in the Sea Urchin
Warner, J. F., Mccarthy, A. M., Morris, R. L., & McClay, D. R. (2016)
Simple Method To Characterize the Ciliary Proteome of Multiciliated Cells
Sim, H. J., Yun, S., Kim, H. E., Kwon, K. Y., Kim, G., Yun, S., Kim, B. G., Myung, K., Park, T. J., & Kwon, T. (2019) · Journal of Proteome Research · doi:10.1021/acs.jproteome.9b00589 · Cited by 16 · see citing works
Letter Hedgehog Signaling Requires Motile Cilia in the Sea Urchin
Warner, J. F., Mccarthy, A. M., Morris, R. L., & McClay, D. R. (2016)

Authors: Sigg, M. A., Menchen, T., Lee, C., Johnson, J., Jungnickel, M. K., Choksi, S. P., Garcia, G., Busengdal, H., Dougherty, G. W., Pennekamp, P., Werner, C., Rentzsch, F., Florman, H. M., Krogan, N., Wallingford, J. B., Omran, H., & Reiter, J. F.
Affiliations: University of California, San Francisco (US)
University of Münster (DE)
The University of Texas at Austin (US)
University of Massachusetts Chan Medical School (US)
University of Bergen (NO)
Gladstone Institutes (US)
Corresponding author: Reiter, Jeremy F.
ORCID: Sigg, Monika Abedin
Lee, Chanjae
Jungnickel, Melissa K.
Choksi, Semil P.
Dougherty, Gerard W.
Pennekamp, Petra
Rentzsch, Fabian
Florman, Harvey M.
Krogan, Nevan
Wallingford, John B.
Omran, Heymut
Reiter, Jeremy F.
Venue: Developmental Cell
Publisher: Elsevier BV
Published: 2017-12
Volume: 43
Issue: 6
Pages: 744-762.e11
ISSN: 1534-5807 (ISSN-L)
DOI: 10.1016/j.devcel.2017.11.014
PMC: PMC5752135
OpenAlex: W2778987076
Cited by: 130
References: 144
Citations by year: 2026: 11 · 2025: 16 · 2024: 11 · 2023: 13 · 2022: 16 · 2021: 13 · 2020: 20 · 2019: 22 · 2018: 6 · 2017: 1 · 2014: 1
FWCI: 8.87
Type: journal article
Language: en
Open access: bronze
doi.org
Licence: www.elsevier.com/tdm/userlicense/1.0/ (tdm)
www.elsevier.com/open-access/userlicense/1.0/ (vor, 382 d)
Locations: Developmental Cell (publishedVersion)
bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
PubMed (publishedVersion)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
eScholarship (California Digital Library) (submittedVersion)
Funders: NIH (AR054396, GM095941, HD046948, HD054418)
Burroughs Wellcome Fund
Packard Foundation
Sandler Family Supporting Foundation
Deutsche Forschungsgemeinschaft
Interdisziplinären Zentrum für Klinische Forschung Muenster (Om2/009/12, Om2/015/16)
European Commission (262055, GA 241955, GA 305404)
Eva Luise und Horst Köhler Stiftung
Kindness for Kids
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and Kidney Cyst Diseases
Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Cystic Fibrosis Research Advances
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Hedgehog Signaling Pathway Studies
Keywords: cilia, ciliary proteome, evolutionary conservation, Hedgehog signaling, G protein-coupled receptors, TRP channels, motile cilia, situs inversus, sea urchins, sea anemone, choanoflagellates
MeSH terms: Animals, Calmodulin-Binding Proteins, Cilia, Humans, Mutation, Phylogeny, Sea Anemones, Sea Urchins, Xenopus laevis, Zebrafish, Organelles, Signal Transduction, Cell Culture Techniques, Proteomics, Receptors, G-Protein-Coupled, Adaptor Proteins, Signal Transducing, Transient Receptor Potential Channels, Mice, Hedgehog Proteins, Choanoflagellata

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Evolutionary Proteomics Uncovers Ancient Associations of Cilia with Signaling Pathways

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