Evolutionary Proteomics Uncovers Ancient Associations of Cilia with Signaling Pathways
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 con...
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| Published in | Developmental cell Vol. 43; no. 6; pp. 744 - 762.e11 |
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| Main Authors | , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
18.12.2017
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| Subjects | |
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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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•Evolutionary proteomics identifies conserved ciliary proteins•Ciliary regulators of Hh, GPCR, and TRP channel signaling evolved before bilateria•ENKUR localizes to motile cilia and is required for left-right axis patterning•Mutation of ENKUR causes situs inversus in humans
Cilia are cellular appendages used for motility and intercellular communication. Sigg et al. reconstruct the evolutionary ancestry of cilia through proteomics of sea urchin, sea anemone, and choanoflagellate cilia. One identified ciliary protein, ENKUR, helps pattern the vertebrate left-right body axis. Humans with inherited mutations in ENKUR have situs inversus. |
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| AbstractList | 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 Hh and GPCR pathways were linked to cilia before the origin of bilateria and 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 controls development and human disease.
Cilia are cellular appendages used for motility and intercellular communication. Sigg et al. reconstruct the evolutionary ancestry of cilia through proteomics of sea urchin, sea anemone, and choanoflagellate cilia. One identified ciliary protein, ENKUR, helps pattern the vertebrate left/right body axis. Humans with inherited mutations in ENKUR have situs inversus. 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. 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. [Display omitted] •Evolutionary proteomics identifies conserved ciliary proteins•Ciliary regulators of Hh, GPCR, and TRP channel signaling evolved before bilateria•ENKUR localizes to motile cilia and is required for left-right axis patterning•Mutation of ENKUR causes situs inversus in humans Cilia are cellular appendages used for motility and intercellular communication. Sigg et al. reconstruct the evolutionary ancestry of cilia through proteomics of sea urchin, sea anemone, and choanoflagellate cilia. One identified ciliary protein, ENKUR, helps pattern the vertebrate left-right body axis. Humans with inherited mutations in ENKUR have situs inversus. |
| Author | Krogan, Nevan Omran, Heymut Lee, Chanjae Johnson, Jeffery Menchen, Tabea Florman, Harvey M. Werner, Claudius Jungnickel, Melissa K. Wallingford, John B. Busengdal, Henriette Dougherty, Gerard W. Sigg, Monika Abedin Pennekamp, Petra Rentzsch, Fabian Reiter, Jeremy F. Choksi, Semil P. Garcia, Galo |
| AuthorAffiliation | 7 Department of Cellular and Molecular Pharmacology, University of California, San Francisco, CA 94158, USA 6 Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen 5008, Norway 1 Department of Biochemistry and Biophysics, Cardiovascular Research Institute, University of California, San Francisco, CA 94158, USA 5 University of Massachusetts Medical School, Worcester, MA, 01655, USA 3 Department of Molecular Biosciences, Center for Systems and Synthetic Biology and Institute for Cellular and Molecular Biology, University of Texas at Austin, Austin, TX 78712, USA 2 Department of General Pediatrics, University of Muenster, Muenster 48149, Germany 4 Gladstone Institute of Cardiovascular Disease and Gladstone Institute of Virology and Immunology, San Francisco, CA 94158, USA |
| AuthorAffiliation_xml | – name: 1 Department of Biochemistry and Biophysics, Cardiovascular Research Institute, University of California, San Francisco, CA 94158, USA – name: 3 Department of Molecular Biosciences, Center for Systems and Synthetic Biology and Institute for Cellular and Molecular Biology, University of Texas at Austin, Austin, TX 78712, USA – name: 4 Gladstone Institute of Cardiovascular Disease and Gladstone Institute of Virology and Immunology, San Francisco, CA 94158, USA – name: 6 Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen 5008, Norway – name: 2 Department of General Pediatrics, University of Muenster, Muenster 48149, Germany – name: 7 Department of Cellular and Molecular Pharmacology, University of California, San Francisco, CA 94158, USA – name: 5 University of Massachusetts Medical School, Worcester, MA, 01655, USA |
| Author_xml | – sequence: 1 givenname: Monika Abedin surname: Sigg fullname: Sigg, Monika Abedin organization: Department of Biochemistry and Biophysics, Cardiovascular Research Institute, University of California, San Francisco, CA 94158, USA – sequence: 2 givenname: Tabea surname: Menchen fullname: Menchen, Tabea organization: Department of General Pediatrics, University Children’s Hospital Muenster, Muenster 48149, Germany – sequence: 3 givenname: Chanjae surname: Lee fullname: Lee, Chanjae organization: Department of Molecular Biosciences, Center for Systems and Synthetic Biology and Institute for Cellular and Molecular Biology, University of Texas at Austin, Austin, TX 78712, USA – sequence: 4 givenname: Jeffery surname: Johnson fullname: Johnson, Jeffery organization: Gladstone Institute of Cardiovascular Disease and Gladstone Institute of Virology and Immunology, San Francisco, CA 94158, USA – sequence: 5 givenname: Melissa K. surname: Jungnickel fullname: Jungnickel, Melissa K. organization: Department of Cell and Developmental Biology, University of Massachusetts Medical School, Worcester, MA 01655, USA – sequence: 6 givenname: Semil P. surname: Choksi fullname: Choksi, Semil P. organization: Department of Biochemistry and Biophysics, Cardiovascular Research Institute, University of California, San Francisco, CA 94158, USA – sequence: 7 givenname: Galo surname: Garcia fullname: Garcia, Galo organization: Department of Biochemistry and Biophysics, Cardiovascular Research Institute, University of California, San Francisco, CA 94158, USA – sequence: 8 givenname: Henriette surname: Busengdal fullname: Busengdal, Henriette organization: Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen 5008, Norway – sequence: 9 givenname: Gerard W. surname: Dougherty fullname: Dougherty, Gerard W. organization: Department of General Pediatrics, University Children’s Hospital Muenster, Muenster 48149, Germany – sequence: 10 givenname: Petra surname: Pennekamp fullname: Pennekamp, Petra organization: Department of General Pediatrics, University Children’s Hospital Muenster, Muenster 48149, Germany – sequence: 11 givenname: Claudius surname: Werner fullname: Werner, Claudius organization: Department of General Pediatrics, University Children’s Hospital Muenster, Muenster 48149, Germany – sequence: 12 givenname: Fabian surname: Rentzsch fullname: Rentzsch, Fabian organization: Sars International Centre for Marine Molecular Biology, University of Bergen, Bergen 5008, Norway – sequence: 13 givenname: Harvey M. surname: Florman fullname: Florman, Harvey M. organization: Department of Cell and Developmental Biology, University of Massachusetts Medical School, Worcester, MA 01655, USA – sequence: 14 givenname: Nevan surname: Krogan fullname: Krogan, Nevan organization: Gladstone Institute of Cardiovascular Disease and Gladstone Institute of Virology and Immunology, San Francisco, CA 94158, USA – sequence: 15 givenname: John B. surname: Wallingford fullname: Wallingford, John B. organization: Department of Molecular Biosciences, Center for Systems and Synthetic Biology and Institute for Cellular and Molecular Biology, University of Texas at Austin, Austin, TX 78712, USA – sequence: 16 givenname: Heymut surname: Omran fullname: Omran, Heymut organization: Department of General Pediatrics, University Children’s Hospital Muenster, Muenster 48149, Germany – sequence: 17 givenname: Jeremy F. surname: Reiter fullname: Reiter, Jeremy F. email: jeremy.reiter@ucsf.edu organization: Department of Biochemistry and Biophysics, Cardiovascular Research Institute, University of California, San Francisco, CA 94158, USA |
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| Keywords | cilium TRP channel left-right axis patterning proteomics Hedgehog signaling GPCR sea urchin sea anemone choanoflagellate ciliopathy |
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| SubjectTerms | Adaptor Proteins, Signal Transducing - genetics Adaptor Proteins, Signal Transducing - metabolism Animals Calmodulin-Binding Proteins - genetics Calmodulin-Binding Proteins - metabolism Cell Culture Techniques Choanoflagellata - metabolism choanoflagellate Cilia - genetics Cilia - metabolism ciliopathy cilium GPCR Hedgehog Proteins - metabolism Hedgehog signaling Humans left-right axis patterning Mice Mutation Organelles - metabolism Phylogeny proteomics Proteomics - methods Receptors, G-Protein-Coupled - metabolism sea anemone Sea Anemones - metabolism sea urchin Sea Urchins - metabolism Signal Transduction - genetics Signal Transduction - physiology Transient Receptor Potential Channels - metabolism TRP channel Xenopus laevis - metabolism Zebrafish - metabolism |
| Title | Evolutionary Proteomics Uncovers Ancient Associations of Cilia with Signaling Pathways |
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