Crystal structure of human PACRG in complex with MEIG1 reveals roles in axoneme formation and tubulin binding
Open accessPublished version of a preprint
Abstract
The Parkin co-regulated gene protein (PACRG) binds at the inner junction between doublet microtubules of the axoneme, a structure found in flagella and cilia. PACRG binds to the adaptor protein meiosis expressed gene 1 (MEIG1), but how they bind to microtubules is unknown. Here, we report the crystal structure of human PACRG in complex with MEIG1. PACRG adopts a helical repeat fold with a loop that interacts with MEIG1. Using the structure of the axonemal doublet microtubule from the protozoan Chlamydomonas reinhardtii and single-molecule fluorescence microscopy, we propose that PACRG binds to microtubules while simultaneously recruiting free tubulin to catalyze formation of the inner junction. We show that the homologous PACRG-like protein also mediates dual tubulin interactions but does not bind MEIG1. Our findings establish a framework to assess the function of the PACRG family of proteins and MEIG1 in regulating axoneme assembly.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
The multiple contacts of CFAP20 with ciliary axoneme tubulins and PACRG, as well as proximity to CFAP52 and other proteins at or near the inner junction, could explain the degree of conservation of CFAP20.
“The multiple contacts of CFAP20 with ciliary axoneme tubulins and PACRG, as well as proximity to CFAP52 and other proteins at or near the inner junction19–21,71 (Figs. 1b and 8), could explain this degree of conservation.”
From The inner junction protein CFAP20 functions in motile and non-motile cilia and is critical for vision (2022) · cites this paper as [71]
The Results section (page unavailable) places FAP20 (CFAP20) beside PACRG at the inner junction and reports a PACRG loop that interacts with FAP20. It does not establish CFAP20’s multiple tubulin contacts, proximity to CFAP52, or the proposed explanation for CFAP20’s conservation. (LLM, conf=0.85)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
1 retracted
RETRACTED ARTICLE: Parkin and PINK1 mitigate STING-induced inflammation
Sliter, D. A., Martinez, J., Hao, L., Chen, X., Sun, N., Fischer, T. D., Burman, J. L., Li, Y., Zhang, Z., Narendra, D. P., et al. (2018) · Nature · doi:10.1038/s41586-018-0448-9 · Cited by 1,287 · see citing works
RetractedFiji: an open-source platform for biological-image analysis
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2019 · Cited by 66,890 · see citing works
Features and development of Coot
Emsley, P., Lohkamp, B., Scott, W. G., & Cowtan, K. D. (2010) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444910007493 · Cited by 27,510 · see citing works
<i>PHENIX</i> : a comprehensive Python-based system for macromolecular structure solution
Adams, P. D., Afonine, P. V., Bunkóczi, G., Chen, V. B., Davis, I. W., Echols, N., Headd, J. J., Hung, L.-W., Kapral, G. J., Grosse-Kunstleve, R. W., et al. (2010) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444909052925 · Cited by 23,716 · see citing works
<i>Phaser</i> crystallographic software
McCoy, A. J., Grosse-Kunstleve, R. W., Adams, P. D., Winn, M. D., Storoni, L. C., & Read, R. J. (2007) · Journal of Applied Crystallography · doi:10.1107/s0021889807021206 · Cited by 20,612 · see citing works
Kabsch, W. (2010) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444909047337 · Cited by 16,463 · see citing works
Tissue-based map of the human proteome
Uhlén, M., Fagerberg, L., Hallström, B. M., Lindskog, C., Oksvold, P., Mardinoglu, A., Sivertsson, Å., Kampf, C., Sjöstedt, E., Asplund, A., et al. (2015) · Science · doi:10.1126/science.1260419 · Cited by 15,286 · see citing works
Overview of the <i>CCP</i> 4 suite and current developments
Winn, M. D., Ballard, C. C., Cowtan, K. D., Dodson, E. J., Emsley, P., Evans, P. R., Keegan, R. M., Krissinel, E. B., Leslie, A. G. W., McCoy, A., et al. (2011) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s0907444910045749 · Cited by 12,353 · see citing works
Analysis of protein-coding genetic variation in 60,706 humans
Exome Aggregation Consortium, Lek, M., Karczewski, K. J., Minikel, E. V., Samocha, K. E., Banks, E., Fennell, T., O’Donnell-Luria, A. H., Ware, J. S., Hill, A. J., et al. (2016) · Nature · doi:10.1038/nature19057 · Cited by 9,587 · see citing works
Liebschner, D. C., Afonine, P. V., Baker, M. L., Bunkòczi, G., Chen, V. B., Croll, T. I., Hintze, B. J., Hung, L., Jain, S., McCoy, A. J., et al. (2019) · Acta Crystallographica Section D Structural Biology · doi:10.1107/s2059798319011471 · Cited by 6,709 · see citing works
The I-TASSER Suite: protein structure and function prediction
Yang, J., Yan, R., Roy, A., Xu, D., Poisson, J., & Zhang, Y. (2015) · Nature Methods · doi:10.1038/nmeth.3213 · Cited by 5,596 · see citing works
Mutations in the parkin gene cause autosomal recessive juvenile parkinsonism
Kitada, T., Asakawa, S., Hattori, N., Matsumine, H., Yamamura, Y., Minoshima, S., Yokochi, M., Mizuno, Y., & Shimizu, N. (1998) · Nature · doi:10.1038/33416 · Cited by 5,227 · see citing works
Drosophila pink1 is required for mitochondrial function and interacts genetically with parkin
Clark, I. E., Dodson, M. W., Jiang, C., Cao, J. H., Huh, J. R., Seol, J. H., Yoo, S. J., Hay, B. A., & Guo, M. (2006) · Nature · doi:10.1038/nature04779 · Cited by 1,788 · see citing works
Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by parkin
Park, J., Lee, S. B., Lee, S., Kim, Y., Song, S., Kim, S., Bae, E., Kim, J., Shong, M., Kim, J.-M., et al. (2006) · Nature · doi:10.1038/nature04788 · Cited by 1,705 · see citing works
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. (2020) · eLife · doi:10.7554/elife.52760 · Cited by 1,676 · see citing works
Self-citationStructure of the αβ tubulin dimer by electron crystallography
Nogales, E., Wolf, S., & Downing, K. (1998) · Nature · doi:10.1038/34465 · Cited by 1,623 · see citing works
Automated macromolecular model building for X-ray crystallography using ARP/wARP version 7
Langer, G., Cohen, S. X., Lamzin, V. S., & Perrakis, A. (2008) · Nature Protocols · doi:10.1038/nprot.2008.91 · Cited by 1,606 · see citing works
Terwilliger, T. C., Grosse-Kunstleve, R. W., Afonine, P. V., Moriarty, N. W., Zwart, P. H., Hung, L.-W., Read, R. J., & Adams, P. D. (2008) · Acta Crystallographica Section D Biological Crystallography · doi:10.1107/s090744490705024x · Cited by 1,462 · see citing works
Mitochondrial pathology and apoptotic muscle degeneration in <i>Drosophila parkin</i> mutants
Greene, J. C., Whitworth, A. J., Kuo, I., Andrews, L. A., Feany, M. B., & Pallanck, L. J. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0737556100 · Cited by 1,203 · see citing works
Genomewide Association Study of Leprosy
Zhang, F., Huang, W., Chen, S., Sun, L., Liu, H. D., Li, Y., Cui, Y., Yan, X., Yang, H., Yang, R., et al. (2009) · New England Journal of Medicine · doi:10.1056/nejmoa0903753 · Cited by 1,037 · see citing works
Parkin-deficient Mice Exhibit Nigrostriatal Deficits but Not Loss of Dopaminergic Neurons
Goldberg, M. S., Fleming, S. M., Palacino, J. J., Cepeda, C., Lam, H. A., Bhatnagar, A., Meloni, E. G., Wu, N., Ackerson, L. C., Klapstein, G. J., et al. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m308947200 · Cited by 913 · see citing works
Cellular signalling by primary cilia in development, organ function and disease
Anvarian, Z., Mykytyn, K., Mukhopadhyay, S., Pedersen, L. B., & Christensen, S. T. (2019) · Nature Reviews Nephrology · doi:10.1038/s41581-019-0116-9 · Cited by 845 · see citing works
[39] Preparation of modified tubulins
Hyman, A. A., Drechsel, D. N., Kellogg, D., Salser, S. J., Sawin, K. E., Steffen, P., Wordeman, L. G., & Mitchison, T. J. (1991) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/0076-6879(91)96041-o · Cited by 733 · see citing works
Loss of PINK1 causes mitochondrial functional defects and increased sensitivity to oxidative stress
Gautier, C. A., Kitada, T., & Shen, J. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0802076105 · Cited by 698 · see citing works
The ubiquitin ligase parkin mediates resistance to intracellular pathogens
Manzanillo, P. S., Ayres, J. S., Watson, R. O., Collins, A. C., Souza, G., Rae, C. S., Schneider, D. S., Nakamura, K., Shiloh, M. U., & Cox, J. S. (2013) · Nature · doi:10.1038/nature12566 · Cited by 588 · see citing works
Intestinal infection triggers Parkinson's disease-like symptoms in Pink1(-/-) mice
Matheoud, D., Cannon, T., Voisin, A., Penttinen, A.-M., Ramet, L., Fahmy, A. M., Ducrot, C., Laplante, A., Bourque, M.-J., Zhu, L., et al. (2019) · Nature · doi:10.1038/s41586-019-1405-y · Cited by 496 · see citing works
Susceptibility to leprosy is associated with PARK2 and PACRG
Mira, M. T., Alcaïs, A., Thuc, N. V., Moraes, M. O., Flumeri, C. D., Thai, V. H., Phuong, M. C., Hương, N. T., Ba, N. N., Khoa, P. X., et al. (2004) · Nature · doi:10.1038/nature02326 · Cited by 467 · see citing works
Steger, M., Diez, F., Dhekne, H. S., Lis, P., Nirujogi, R. S., Karayel, Ö., Tonelli, F., Martinez, T. N., Lorentzen, E., Pfeffer, S. R., et al. (2017) · eLife · doi:10.7554/elife.31012 · Cited by 465 · see citing works
A Proteomic Analysis of Human Cilia
Ostrowski, L. E., Blackburn, K., Radde, K. M., Moyer, M. B., Schlatzer, D., Moseley, M. A., & Boucher, R. C. (2002) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m200037-mcp200 · Cited by 441 · see citing works
Proteomics of Primary Cilia by Proximity Labeling
Mick, D. U., Rodrigues, R. B., Leib, R. D., Adams, C. M., Chien, A. S., Gygi, S. P., & Nachury, M. V. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.10.015 · Cited by 409 · see citing works
To beat or not to beat: roles of cilia in development and disease
Ibáñez-Tallon, I. (2003) · Human Molecular Genetics · doi:10.1093/hmg/ddg061 · Cited by 349 · see citing works
Pickrell, A. M., Huang, C.-H., Kennedy, S. R., Ordureau, A., Sideris, D. P., Hoekstra, J. G., Harper, J. W., & Youle, R. J. (2015) · Neuron · doi:10.1016/j.neuron.2015.06.034 · Cited by 327 · see citing works
Recognition of RNA polymerase II carboxy-terminal domain by 3′-RNA-processing factors
Meinhart, A., & Cramer, P. (2004) · Nature · doi:10.1038/nature02679 · Cited by 315 · see citing works
Structure of the Decorated Ciliary Doublet Microtubule
Ma, M., Stoyanova, M., Rademacher, G., Dutcher, S. K., Brown, A., & Zhang, R. (2019) · Cell · doi:10.1016/j.cell.2019.09.030 · Cited by 290 · see citing works
Continuous directed evolution of aminoacyl-tRNA synthetases
Bryson, D. I., Fan, C., Guo, L., Miller, C. A., Söll, D. G., & Liu, D. R. (2017) · Nature Chemical Biology · doi:10.1038/nchembio.2474 · Cited by 267 · see citing works
Microtubule Dynamics Reconstituted In Vitro and Imaged by Single-Molecule Fluorescence Microscopy
Gell, C., Bormuth, V., Brouhard, G. J., Cohen, D. N., Diez, S., Friel, C. T., Helenius, J. H., Nitzsche, B., Petzold, H., Ribbe, J., et al. (2010) · Methods in cell biology · doi:10.1016/s0091-679x(10)95013-9 · Cited by 255 · see citing works
Self-citationDhekne, H. S., Yanatori, I., Gomez, R. C., Tonelli, F., Diez, F., Schüle, B., Steger, M., Alessi, D. R., & Pfeffer, S. R. (2018) · eLife · doi:10.7554/elife.40202 · Cited by 240 · see citing works
The E3 Ligase Parkin Maintains Mitochondrial Integrity by Increasing Linear Ubiquitination of NEMO
Müller-Rischart, A. K., Pilsl, A., Beaudette, P., Patra, M., Hadian, K., Funke, M., Peis, R., Deinlein, A., Schweimer, C., Kuhn, P., et al. (2013) · Molecular Cell · doi:10.1016/j.molcel.2013.01.036 · Cited by 210 · see citing works
A Missense LRRK2 Variant Is a Risk Factor for Excessive Inflammatory Responses in Leprosy
Fava, V. M., Manry, J., Cobat, A., Orlova, M., Thuc, N. V., Ba, N. N., Thai, V. H., Abel, L., Alcaïs, A., Schurr, E., et al. (2016) · PLoS neglected tropical diseases · doi:10.1371/journal.pntd.0004412 · Cited by 205 · see citing works
Dynamic and redundant regulation of LRRK2 and LRRK1 expression
Biskup, S., Moore, D. J., Rea, A., Lorenz-Deperieux, B., Coombes, C. E., Dawson, V. L., Dawson, T. M., & West, A. B. (2007) · BMC Neuroscience · doi:10.1186/1471-2202-8-102 · Cited by 159 · see citing works
Three-dimensional architecture of epithelial primary cilia
Sun, S., Fisher, R. L., Bowser, S. S., Pentecost, B. T., & Sui, H. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1821064116 · Cited by 142 · see citing works
Doublecortin Recognizes the 13-Protofilament Microtubule Cooperatively and Tracks Microtubule Ends
Bechstedt, S., & Brouhard, G. J. (2012) · Developmental Cell · doi:10.1016/j.devcel.2012.05.006 · Cited by 141 · see citing works
Self-citationThe site-specific incorporation of p-iodo-L-phenylalanine into proteins for structure determination
Xie, J., Wang, L., Wu, N., Brock, A., Spraggon, G., & Schultz, P. G. (2004) · Nature Biotechnology · doi:10.1038/nbt1013 · Cited by 135 · see citing works
Structure and Function of Parkin, PINK1, and DJ-1, the Three Musketeers of Neuroprotection
Trempe, J., & Fon, E. A. (2013) · Frontiers in Neurology · doi:10.3389/fneur.2013.00038 · Cited by 130 · see citing works
Self-citationDeficiency of SPAG16L Causes Male Infertility Associated with Impaired Sperm Motility1
Zhang, Z., Kostetskii, I., Tang, W., Haig-Ladewig, L. A., Sapiro, R., Wei, Z., Patel, A. M., Bennett, J., Gerton, G. L., Moss, S. B., et al. (2005) · Biology of Reproduction · doi:10.1095/biolreprod.105.049254 · Cited by 121 · see citing works
Identification of a Novel Gene Linked to Parkin via a Bi-directional Promoter
West, A. B., Lockhart, P. J., O’Farrell, C., & Farrer, M. J. (2003) · Journal of Molecular Biology · doi:10.1016/s0022-2836(02)01376-1 · Cited by 119 · see citing works
Mechanisms of PINK1, ubiquitin and Parkin interactions in mitochondrial quality control and beyond
Bayne, A. N., & Trempe, J. (2019) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-019-03203-4 · Cited by 113 · see citing works
Self-citationSustained Elongation of Sperm Tail Promoted by Local Remodeling of Giant Mitochondria in Drosophila
Noguchi, T., Koizumi, M., & Hayashi, S. (2011) · Current Biology · doi:10.1016/j.cub.2011.04.016 · Cited by 105 · see citing works
Dawe, H. R., Farr, H., Portman, N., Shaw, M. K., & Keith Gull, B. (2005) · Journal of Cell Science · doi:10.1242/jcs.02659 · Cited by 95 · see citing works
Deletion of the Parkin coregulated gene causes male sterility in the quaking viable mouse mutant
Lorenzetti, D., Bishop, C. E., & Justice, M. J. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0401832101 · Cited by 93 · see citing works
The Structure and Dynamics of C. elegans Tubulin Reveals the Mechanistic Basis of Microtubule Growth
Chaaban, S., Jariwala, S., Hsu, C.-T., Redemann, S., Kollman, J. M., Müller-Reichert, T., Sept, D., Bui, K. H., & Brouhard, G. J. (2018) · Developmental Cell · doi:10.1016/j.devcel.2018.08.023 · Cited by 83 · see citing works
Self-citationMEIG1 is essential for spermiogenesis in mice
Zhang, Z., Shen, X., Gude, D., Wilkinson, B. M., Justice, M. J., Flickinger, C. J., Herr, J. C., Eddy, E. M., & Strauss, J. F. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0906414106 · Cited by 81 · see citing works
Imai, Y., Soda, M., Murakami, T., Shoji, M., Abe, K., & Takahashi, R. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m309655200 · Cited by 73 · see citing works
Dymek, E. E., Lin, J., Fu, G., Porter, M. E., Nicastro, D., & Smith, E. F. (2019) · Molecular Biology of the Cell · doi:10.1091/mbc.e19-01-0063 · Cited by 61 · see citing works
Pleiotropic effects for Parkin and LRRK2 in leprosy type-1 reactions and Parkinson’s disease
Fava, V. M., Xu, Y. Z., Lettre, G., Thuc, N. V., Orlova, M., Thai, V. H., Tao, S., Croteau, N., Eldeeb, M. A., MacDougall, E. J., et al. (2019) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1901805116 · Cited by 59 · see citing works
Self-citationA MEIG1/PACRG complex in the manchette is essential for building the sperm flagella
Li, W., Tang, W., Teves, M. E., Zhang, Z., Zhang, L., Li, H., Archer, K. J., Peterson, D. L., Williams, D. C., Strauss, J. F., et al. (2015) · Development · doi:10.1242/dev.119834 · Cited by 58 · see citing works
The role of Rab GTPases in the pathobiology of Parkinson’ disease
Bonet‐Ponce, L., & Cookson, M. R. (2019) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2019.03.009 · Cited by 56 · see citing works
Gazea, M., Tasouri, E., Tolve, M., Bosch, V., Kabanova, A., Gojak, C., Kurtulmus, B., Novikov, O., Spatz, J. P., Pereira, G., et al. (2015) · Developmental Biology · doi:10.1016/j.ydbio.2015.10.033 · Cited by 54 · see citing works
The rat pituitary cleft: A correlated study by scanning and transmission electron microscopy
CORRER, S., & Motta, P. M. (1981) · Cell and Tissue Research · doi:10.1007/bf00233528 · Cited by 46 · see citing works
Ikeda, K., Ikeda, T., Morikawa, K., & Kamiya, R. (2007) · Cell Motility and the Cytoskeleton · doi:10.1002/cm.20225 · Cited by 38 · see citing works
Taylor, J. M., Song, Y. J. C., Huang, Y. M., Farrer, M. J., Delatycki, M. B., Halliday, G. M., & Lockhart, P. J. (2007) · Neurobiology of Disease · doi:10.1016/j.nbd.2007.04.014 · Cited by 36 · see citing works
Parkin‐co‐regulated gene (PACRG) product interacts with tubulin and microtubules
Ikeda, T. (2008) · FEBS Letters · doi:10.1016/j.febslet.2008.02.081 · Cited by 29 · see citing works
Meig1 deficiency causes a severe defect in mouse spermatogenesis
Salzberg, Y., Eldar, T. M. T., Karminsky, O.-D., Itach, S. B., Pietrokovski, S., & Don, J. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.11.028 · Cited by 24 · see citing works
Stephenson, S. E. M., Aumann, T. D., Taylor, J. M., Riseley, J. R., Li, R., Mann, J. R., Tomas, D., & Lockhart, P. J. (2018) · Scientific Reports · doi:10.1038/s41598-018-25766-1 · Cited by 24 · see citing works
The parkin-coregulated gene product PACRG promotes TNF signaling by stabilizing LUBAC
Meschede, J., Šadič, M., Furthmann, N., Miedema, T., Sehr, D. A., Müller-Rischart, A. K., Bader, V., Berlemann, L. A., Pilsl, A., Schlierf, A., et al. (2020) · Science Signaling · doi:10.1126/scisignal.aav1256 · Cited by 24 · see citing works
PACRG, a protein linked to ciliary motility, mediates cellular signaling
Loucks, C. M., Bialas, N. J., Dekkers, M. P. J., Walker, D. S., Grundy, L. J., Li, C., Inglis, P. N., Kida, K., Schafer, W. R., Blacque, O. E., et al. (2016) · Molecular Biology of the Cell · doi:10.1091/mbc.e15-07-0490 · Cited by 23 · see citing works
Wilson, G. R. A., Tan, J., Brody, K. M., Taylor, J. M., Delatycki, M. B., & Lockhart, P. J. (2009) · Neuroscience Letters · doi:10.1016/j.neulet.2009.05.043 · Cited by 20 · see citing works
Evolution of Closely Linked Gene Pairs in Vertebrate Genomes
Franck, E., Hulsen, T., Huynen, M. A., JONG, W. W. D., Lubsen, N. H., & Madsen, O. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn136 · Cited by 18 · see citing works
Dissecting the structural basis of MEIG1 interaction with PACRG
Li, W., Walavalkar, N. M., Buchwald, W. A., Teves, M. E., Zhang, L., Liu, H. D., Bilinovich, S. M., Peterson, D. L., Strauss, J. F., Williams, D. C., Jr., et al. (2016) · Scientific Reports · doi:10.1038/srep18278 · Cited by 14 · see citing works
Preparation of Tubulin from Porcine Brain
Ashford, A. J., & Hyman, A. A. (2006) · Cell Biology · doi:10.1016/b978-012164730-8/50094-0 · Cited by 14 · see citing works
Li, D., Yu, J., Chen, Y., Ma, H.-B., Wang, Z., Zhu, Y., & Zhang, X. (2004) · Acta Biochimica et Biophysica Sinica · doi:10.1093/abbs/36.2.141 · Cited by 10 · see citing works
Nakakura, T., Suzuki, T., Horiguchi, K., Fujiwara, K., Tsukada, T., Asano-Hoshino, A., Tanaka, H., Arisawa, K., Nishijima, Y., Nekooki-Machida, Y., et al. (2016) · Medical Molecular Morphology · doi:10.1007/s00795-016-0148-1 · Cited by 10 · see citing works
A microtubule crosslinking protocol for integrative structural modeling activities
Rafiei, A., & Schriemer, D. C. (2019) · Analytical Biochemistry · doi:10.1016/j.ab.2019.113416 · Cited by 5 · see citing works
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
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
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. (2020) · eLife · doi:10.7554/elife.52760 · Cited by 1,676 · see citing works
Self-citationStructurally divergent and recurrently mutated regions of primate genomes
(2024) · doi:10.1016/j.cell.2024.01.052 · Cited by 73 · see citing works
“62–64 One of the regions classified as an SDR was the D4Z4 repeat locus—a region associated with the double homeobox 4 gene ( DUX4 ) and facioscapulohumeral muscular dystrophy when mis-expressed in humans.”
Structural Mechanisms of Mitochondrial Quality Control Mediated by PINK1 and Parkin
Trempe, J., & Gehring, K. (2023) · Journal of Molecular Biology · doi:10.1016/j.jmb.2023.168090 · Cited by 58 · see citing works
Self-citationEpendymal cells and neurodegenerative disease: outcomes of compromised ependymal barrier function
Nelles, D. G., & Hazrati, L. (2022) · Brain Communications · doi:10.1093/braincomms/fcac288 · Cited by 46 · see citing works
Chrystal, P. W., Lambacher, N. J., Doucette, L. P., Bellingham, J., Schiff, E. R., Noel, N. C. L., Li, C., Tsiropoulou, S., Casey, G. A., Zhai, Y., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-33820-w · Cited by 31 · see citing works
TCFL5 deficiency impairs the pachytene to diplotene transition during spermatogenesis in the mouse
Galán‐Martínez, J., Berenguer, I., Maza, M. D. C. L., Stamatakis, K., Gironès, N., & Fresno, M. (2022) · Scientific Reports · doi:10.1038/s41598-022-15167-w · Cited by 28 · see citing works
FAP106 is an interaction hub for assembling microtubule inner proteins at the cilium inner junction
Shimogawa, M. M., Wijono, A. S., Wang, H., Zhang, J., Sha, J., Szombathy, N., Vadakkan, S., Pelayo, P., Jonnalagadda, K., Wohlschlegel, J., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-40230-z · Cited by 18 · see citing works
“Some organisms have multiple PACRG homologs 17,41,52 .”
Modulation of inner junction proteins contributes to axoneme differentiation
Chen, Z., Li, M., Zhu, H., & Ou, G. (2023) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2303955120 · Cited by 18 · see citing works
“In support of these imaging and genetic results, the in vitro biochemical data show that the human PACRG proteins bind to MTs and recruit tubulin (50), suggesting that PCRG-1 alone may promote axoneme doublet formation.”
ResultMotile Cilia in Female and Male Reproductive Tracts and Fertility
Włoga, D., Joachimiak, E., Osinka, A., Ahmadi, S., & Majhi, S. (2024) · Cells · doi:10.3390/cells13231974 · Cited by 13 · see citing works
Khan, A. H., Lee, L. K., & Smith, D. (2022) · Translational Neuroscience · doi:10.1515/tnsci-2022-0237 · Cited by 11 · see citing works
Li, W., Huang, Q., Zhang, L., Liu, H., Zhang, D., Yuan, S., Yap, Y., Qü, W., Shiang, R., Song, S., et al. (2021) · Journal of Biological Chemistry · doi:10.1016/j.jbc.2021.101312 · Cited by 9 · see citing works
“The structure of human MEIG1/PACRG complex has been recently solved, including identification of the key amino acids on PACRG protein that mediate the MEIG1/ PACRG interaction (48).”
BackgroundMicrotubule inner proteins – bridging structure and function in ciliary biology
Gui, M., & Orbach, R. (2025) · Journal of Cell Science · doi:10.1242/jcs.264192 · Cited by 8 · see citing works
An, J., Wang, J., Kong, S., Shi, S., Chen, W., Yuan, P., He, Q., Chen, Y., Li, Y., Yang, Y., et al. (2023) · Genomics Proteomics & Bioinformatics · doi:10.1093/gpbjnl/qzad004 · Cited by 7 · see citing works
“And loss of PACRG can cause male sterility [34].”
BackgroundSARS-CoV-2 infection results in a unique lung proteome long after virus resolution in the hamster
Boese, A. S., Warner, B. M., McQueen, P., Vendramelli, R., Tailor, N., Griffin, B. D., Chan, M., Audet, J., Leung, A., McCorrister, S. J., et al. (2024) · npj Viruses · doi:10.1038/s44298-024-00049-x · Cited by 5 · see citing works
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
Self-citationFunctional Expression, Purification and Identification of Interaction Partners of PACRG
Liu, T., Zhao, H., Jian, S., Gong, S., Li, S., Ma, Y., Chen, J., & Liu, W. (2021) · Molecules · doi:10.3390/molecules26082308 · Cited by 4 · see citing works
“Additionally, their results showed that expression of GST-fused PACRG formed inclusion bodies by using the pGEX-6p1 vector [16].”
BackgroundMethodInfluentialCryo-electron tomography of eel sperm flagella reveals a molecular “minimum system” for motile cilia
Schrad, J. R., Fu, G., Hable, W. E., Tayar, A. M., Oliveira, K., & Nicastro, D. (2024) · Molecular Biology of the Cell · doi:10.1091/mbc.e24-08-0351 · Cited by 5 · see citing works
“To determine whether the eel may have lost a second PACRG protein during its evolutionary history, we searched for PACRG proteins across bony fish ( Actinopterygii ) using NCBI’s BLAST algorithm (Altschul et al. , 1990), but we did not find instances of multiple PACRG proteins, suggesting that the ancestral eel did not…”
InfluentialMolecular dynamics study reveals key disruptors of MEIG1–PACRG interaction
Hasse, T., Zhang, Z., & Huang, Y. M. (2022) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.26449 · Cited by 3 · see citing works
Hasse, T., Zhang, Z., & Huang, Y. M. (2025) · Proteins Structure Function and Bioinformatics · doi:10.1002/prot.26829 · Cited by 1 · see citing works
Microtubule Inner Protein CFAP77 Contributes to Sperm Motility and Male Fertility in Mice
Wang, H., Pham, A. H., Luo, M., Ikawa, M., & Miyata, H. (2025) · Andrology · doi:10.1111/andr.70152 · Cited by 1 · see citing works
“The inner junction of the A-tubule and B-tubule is linked by CFAP20 [9, 10] and PACRG [11, 12], while the outer junction is thought to be formed by a direct interaction between protofilaments.”
Engstler, M., & Morriswood, B. (2020) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.737227664.793579388
Methods for the localization of cellular components in Chlamydomonas
Silflow, C. D., Mackinder, L. C. M., & Wingfield, J. L. (2023) · Elsevier eBooks · doi:10.1016/b978-0-12-822457-1.00003-0
A Cross Talk Between Natural Biomolecules and Neuroglia
Iman, T., Akram, R., Tehreem, A., Asghar, A., Mustafa, M., & Iqbal, J. (2026) · IGI Global eBooks · doi:10.4018/979-8-3373-4139-2.ch001
- Authors
- Khan, N., Pelletier, D., McAlear, T. S., Croteau, N., Veyron, S., Bayne, A. N., Black, C., Ichikawa, M., Khalifa, A. A. Z., Chaaban, S., Kurinov, I., Brouhard, G., Bechstedt, S., Bui, K. H., & Trempe, J.-F.
- Affiliations
- McGill University (CA)
- Cornell University (US)
- Corresponding author
- Trempe, Jean-François
- ORCID
- Venue
- Structure
- Publisher
- Elsevier BV
- Published
- 2021-06
- Volume
- 29
- Issue
- 6
- Pages
- 572-586.e6
- ISSN
- 0969-2126 (ISSN-L)
- PMC
- PMC8178172
- OpenAlex
- W3126256293
- Cited by
- 24
- References
- 74
- Citations by year
- 2026: 1 · 2025: 3 · 2024: 4 · 2023: 6 · 2022: 5 · 2021: 2 · 2020: 2 · 2019: 1
- FWCI
- 2.40
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- www.elsevier.com/tdm/userlicense/1.0/ (tdm)
- www.elsevier.com/legal/tdmrep-license (tdm)
- www.elsevier.com/open-access/userlicense/1.0/ (vor, 367 d)
- doi.org/10.15223/policy-017 (stm-asf)
- doi.org/10.15223/policy-037 (stm-asf)
- doi.org/10.15223/policy-012 (stm-asf)
- doi.org/10.15223/policy-029 (stm-asf)
- doi.org/10.15223/policy-004 (stm-asf)
- Locations
- Structure (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- Natural Sciences and Engineering Research Council of Canada
- National Institute of General Medical Sciences
- Canadian Institutes of Health Research
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic and Kidney Cyst Diseases
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Microtubule and mitosis dynamics
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Cystic Fibrosis Research Advances
- Keywords
- PACRG, axoneme assembly, tubulin binding, flagella, cilia, Chlamydomonas reinhardtii, protein-protein complex
- MeSH terms
- Protein Domains, Single Molecule Imaging, Binding Sites, Humans, Microfilament Proteins, Microscopy, Fluorescence, Mutation, Nuclear Proteins, Phosphoproteins, Protein Binding, Protein Conformation, Tubulin, Chlamydomonas reinhardtii, Crystallography, X-Ray, Cell Cycle Proteins, Molecular Chaperones, Multiprotein Complexes, Axoneme
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
