The Origin of GPCRs: Identification of Mammalian like Rhodopsin, Adhesion, Glutamate and Frizzled GPCRs in Fungi
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G protein-coupled receptors (GPCRs) in humans are classified into the five main families named Glutamate, Rhodopsin, Adhesion, Frizzled and Secretin according to the GRAFS classification. Previous results show that these mammalian GRAFS families are well represented in the Metazoan lineages, but they have not been shown to be present in Fungi. Here, we systematically mined 79 fungal genomes and provide the first evidence that four of the five main mammalian families of GPCRs, namely Rhodopsin, Adhesion, Glutamate and Frizzled, are present in Fungi and found 142 novel sequences between them. Significantly, we provide strong evidence that the Rhodopsin family emerged from the cAMP receptor family in an event close to the split of Opisthokonts and not in Placozoa, as earlier assumed. The Rhodopsin family then expanded greatly in Metazoans while the cAMP receptor family is found in 3 invertebrate species and lost in the vertebrates. We estimate that the Adhesion and Frizzled families evolved before the split of Unikonts from a common ancestor of all major eukaryotic lineages. Also, the study highlights that the fungal Adhesion receptors do not have N-terminal domains whereas the fungal Glutamate receptors have a broad repertoire of mammalian-like N-terminal domains. Further, mining of the close unicellular relatives of the Metazoan lineage, Salpingoeca rosetta and Capsaspora owczarzaki, obtained a rich group of both the Adhesion and Glutamate families, which in particular provided insight to the early emergence of the N-terminal domains of the Adhesion family. We identified 619 Fungi specific GPCRs across 79 genomes and revealed that Blastocladiomycota and Chytridiomycota phylum have Metazoan-like GPCRs rather than the GPCRs specific for Fungi. Overall, this study provides the first evidence of the presence of four of the five main GRAFS families in Fungi and clarifies the early evolutionary history of the GPCR superfamily.
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MrBayes 3: Bayesian phylogenetic inference under mixed models
Ronquist, F., & Huelsenbeck, J. P. (2003) · Bioinformatics · doi:10.1093/bioinformatics/btg180 · Cited by 28,956 · see citing works
Guindon, S., Dufayard, J.-F., Lefort, V., Anisimova, M., Hordijk, W., & Gascuel, O. (2010) · Systematic Biology · doi:10.1093/sysbio/syq010 · Cited by 18,376 · see citing works
The Pfam Protein Families Database
Bateman, A. G. (2002) · Nucleic Acids Research · doi:10.1093/nar/30.1.276 · Cited by 14,062 · see citing works
Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences
Li, W.-Z., & Godzik, A. (2006) · Bioinform. · doi:10.1093/bioinformatics/btl158 · Cited by 10,994 · see citing works
Eddy, S. R. (1998) · Bioinformatics · doi:10.1093/bioinformatics/14.9.755 · Cited by 5,515 · see citing works
MAFFT version 5: improvement in accuracy of multiple sequence alignment
Katoh, K., Kuma, K., Toh, H., & Miyata, T. (2005) · Nucleic Acids Research · doi:10.1093/nar/gki198 · Cited by 5,063 · see citing works
Genome Sequence of the Nematode C. elegans : A Platform for Investigating Biology
Berg, J. (1998) · Science · doi:10.1126/science.282.5396.2012 · Cited by 4,458 · see citing works
Fredriksson, R., Lagerström, M. C., Lundin, L.-G., & Schiöth, H. B. (2003) · Molecular Pharmacology · doi:10.1124/mol.63.6.1256 · Cited by 2,941 · see citing works
Self-citationThe Pfam protein families database
Finn, R. D., Mistry, J., Tate, J., Coggill, P., Heger, A., Pollington, J. E., Gavin, O. L., Gunasekaran, P., Ceric, G., Forslund, K., et al. (2010) · Nucleic Acids Research · doi:10.1093/nar/gkp985 · Cited by 2,694 · see citing works
The structure and function of G-protein-coupled receptors
Rosenbaum, D. M., Rasmussen, S. G. F., & Kobilka, B. K. (2009) · Nature · doi:10.1038/nature08144 · Cited by 2,534 · see citing works
A Combined Transmembrane Topology and Signal Peptide Prediction Method
Käll, L., Krogh, A., & Sonnhammer, E. L. L. (2004) · Journal of Molecular Biology · doi:10.1016/j.jmb.2004.03.016 · Cited by 2,474 · see citing works
The challenge of emerging and re-emerging infectious diseases
Morens, D. M., Folkers, G. K., & Fauci, A. S. (2004) · Nature · doi:10.1038/nature02759 · Cited by 2,107 · see citing works
The Genome of the Diatom Thalassiosira Pseudonana : Ecology, Evolution, and Metabolism
Armbrust, E. V., Berges, J. A., Bowler, C., Green, B. R., Martínez, D., Putnam, N. H., Zhou, S., Allen, A. E., Apt, K. E., Bechner, M., et al. (2004) · Science · doi:10.1126/science.1101156 · Cited by 2,029 · see citing works
Structural diversity of G protein-coupled receptors and significance for drug discovery
Lagerström, M. C., & Schiöth, H. B. (2008) · Nature Reviews Drug Discovery · doi:10.1038/nrd2518 · Cited by 1,489 · see citing works
Self-citationThe genome of the social amoeba Dictyostelium discoideum
Eichinger, L., Pachebat, J. A., Glöckner, G., Rajandream, M.-A., Sucgang, R., Berriman, M., Song, J., Olsen, R., Szafranski, K., Xu, Q., et al. (2005) · Nature · doi:10.1038/nature03481 · Cited by 1,351 · see citing works
The Trichoplax genome and the nature of placozoans
Srivastava, M., Begovic, E., Chapman, J., Putnam, N. H., Hellsten, U., Kawashima, T., Kuo, A., Mitros, T., Salamov, A., Carpenter, M. L., et al. (2008) · Nature · doi:10.1038/nature07191 · Cited by 889 · see citing works
Trends in the exploitation of novel drug targets
Rask-Andersen, M., Almén, M. S., & Schiöth, H. B. (2011) · Nature Reviews Drug Discovery · doi:10.1038/nrd3478 · Cited by 853 · see citing works
Self-citationGlobal trends of whole-genome duplications revealed by the ciliate Paramecium tetraurelia
Aury, J., Jaillon, O., Duret, L., Noël, B., Jubin, C., Porcel, B. M., Segurens, B., Daubin, V., Anthouard, V., Aiach, N. G., et al. (2006) · Nature · doi:10.1038/nature05230 · Cited by 835 · see citing works
G Protein–Coupled Receptor Rhodopsin
Palczewski, K. (2006) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.75.103004.142743 · Cited by 764 · see citing works
Macronuclear Genome Sequence of the Ciliate Tetrahymena thermophila, a Model Eukaryote
Eisen, J. A., Coyne, R. S., Wu, M., Wu, D., Thiagarajan, M., Wortman, J. R., Badger, J. H., Ren, Q., Amedeo, P., Jones, K. M., et al. (2006) · PLoS Biology · doi:10.1371/journal.pbio.0040286 · Cited by 759 · see citing works
The Repertoire of G-Protein–Coupled Receptors in Fully Sequenced Genomes
Fredriksson, R., & Schiöth, H. B. (2005) · Molecular Pharmacology · doi:10.1124/mol.104.009001 · Cited by 613 · see citing works
Self-citationAlmén, M. S., Nordström, K. J. V., Fredriksson, R., & Schiöth, H. B. (2009) · BMC Biology · doi:10.1186/1741-7007-7-50 · Cited by 601 · see citing works
Self-citationA Chemoattractant Receptor Controls Development in Dictyostelium discoideum
Klein, P. S., Sun, T. J., Saxe, C. L., Kimmel, A. R., Johnson, R. L., & Devreotes, P. N. (1988) · Science · doi:10.1126/science.3047871 · Cited by 482 · see citing works
Bjarnadóttir, T. K., Gloriam, D. E. I., Hellstrand, S. H., Kristiansson, H., Fredriksson, R., & Schiöth, H. B. (2006) · Genomics · doi:10.1016/j.ygeno.2006.04.001 · Cited by 433 · see citing works
Self-citationMedina, M., Collins, A. G., Silberman, J. D., & Sogin, M. L. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.171316998 · Cited by 395 · see citing works
Invasive aspergillosis in the intensive care unit
Meersseman, W., Lagrou, K., Maertens, J., & Wijngaerden, E. V. (2007) · Clinical Infectious Diseases · doi:10.1086/518852 · Cited by 366 · see citing works
Heterotrimeric G Protein Signaling in Filamentous Fungi
Li, L., Wright, S. J., Kryštofová, S., Park, G., & Borkovich, K. A. (2007) · Annual Review of Microbiology · doi:10.1146/annurev.micro.61.080706.093432 · Cited by 353 · see citing works
Byrnes, E. J., Li, W., Lewit, Y., Ma, H., Voelz, K., Ren, P., Carter, D. A., Chaturvedi, V., Bildfell, R. J., May, R. C., et al. (2010) · PLoS Pathogens · doi:10.1371/journal.ppat.1000850 · Cited by 330 · see citing works
Fingerprinting G-protein-coupled receptors
Attwood, T. K., & Findlay, J. B. C. (1994) · Protein Engineering Design and Selection · doi:10.1093/protein/7.2.195 · Cited by 302 · see citing works
Drosophila melanogaster G Protein–Coupled Receptors
Brody, T., & Cravchik, A. (2000) · The Journal of Cell Biology · doi:10.1083/jcb.150.2.f83 · Cited by 267 · see citing works
James, T. Y., Litvintseva, A. P., Vilgalys, R. J., Morgan, J. A. T., Taylor, J. W., Fisher, M. C., Berger, L., Weldon, C., Preez, L. D., & Longcore, J. E. (2009) · PLoS Pathogens · doi:10.1371/journal.ppat.1000458 · Cited by 218 · see citing works
Novel G-protein-coupled receptor-like proteins in the plant pathogenic fungus Magnaporthe grisea
Kulkarni, R. D., Thon, M. R., Pan, H. H., & Dean, R. A. (2005) · Genome biology · doi:10.1186/gb-2005-6-3-r24 · Cited by 207 · see citing works
The origins of multicellularity: a multi-taxon genome initiative
Ruiz‐Trillo, I., Burger, G., Holland, P. W. H., King, N., Lang, B. F., Roger, A. J., & Gray, M. W. (2007) · Trends in Genetics · doi:10.1016/j.tig.2007.01.005 · Cited by 206 · see citing works
Magnificent seven: roles of G protein-coupled receptors in extracellular sensing in fungi
Xue, C., Hsueh, Y.-P., & Heitman, J. (2008) · FEMS Microbiology Reviews · doi:10.1111/j.1574-6976.2008.00131.x · Cited by 206 · see citing works
Molecular phylogeny of choanoflagellates, the sister group to Metazoa
Carr, M., Leadbeater, B. S. C., Hassan, R., Nelson, M., & Baldauf, S. L. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0801667105 · Cited by 205 · see citing works
Nordström, K. J. V., Almén, M. S., Edstam, M. M., Fredriksson, R., & Schiöth, H. B. (2011) · Molecular Biology and Evolution · doi:10.1093/molbev/msr061 · Cited by 178 · see citing works
Self-citationHeterotrimeric G protein signaling and RGSs in Aspergillus nidulans.
Yu, J. (2006) · PubMed · Cited by 139 · see citing works
G-protein and cAMP-mediated signaling in aspergilli: A genomic perspective
Lafon, A., Han, K., Seo, J., Yu, J., & d’Enfert, C. (2006) · Fungal Genetics and Biology · doi:10.1016/j.fgb.2006.02.001 · Cited by 137 · see citing works
The Secretin GPCRs Descended from the Family of Adhesion GPCRs
Nordström, K. J. V., Lagerström, M. C., Waller, L. M. J., Fredriksson, R., & Schiöth, H. B. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn228 · Cited by 126 · see citing works
Self-citationThe Dawn of Fungal Pathogen Genomics
Xu, J., Peng, Y., Dickman, M. B., & Sharon, A. (2006) · Annual Review of Phytopathology · doi:10.1146/annurev.phyto.44.070505.143412 · Cited by 117 · see citing works
The repertoire of G protein-coupled receptors in the sea squirt Ciona intestinalis
Narasimhan, K., Aradhyam, G. K., & Manoj, N. (2008) · BMC Evolutionary Biology · doi:10.1186/1471-2148-8-129 · Cited by 106 · see citing works
Nordström, K. J. V., Fredriksson, R., & Schiöth, H. B. (2008) · BMC Evolutionary Biology · doi:10.1186/1471-2148-8-9 · Cited by 88 · see citing works
Self-citationSignaling mechanisms for chemotaxis
Wang, Y., Chen, C., & Iijima, M. (2011) · Development Growth & Differentiation · doi:10.1111/j.1440-169x.2011.01265.x · Cited by 75 · see citing works
Ruiz‐Trillo, I., Lane, C. E., Archibald, J. M., & Roger, A. J. (2006) · Journal of Eukaryotic Microbiology · doi:10.1111/j.1550-7408.2006.00118.x · Cited by 65 · see citing works
Fungal diseases: an evolving public health challenge*
Warnock, D. W. (2006) · Medical Mycology · doi:10.1080/13693780601009493 · Cited by 62 · see citing works
Signalling and sex in the social amoebozoans
O’Day, D. H., & Keszei, A. F. A. (2011) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/j.1469-185x.2011.00200.x · Cited by 45 · see citing works
Silveira, F. P., & Paterson, D. L. (2005) · Current Opinion in Pulmonary Medicine · doi:10.1097/01.mcp.0000159832.20648.70 · Cited by 34 · see citing works
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Allosteric sodium in class A GPCR signaling
Katritch, V., Fenalti, G., Abola, E. E., Roth, B. L., Cherezov, V., & Stevens, R. C. (2014) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2014.03.002 · Cited by 516 · see citing works
International Union of Basic and Clinical Pharmacology. XCIV. Adhesion G Protein–Coupled Receptors
Hamann, J., Aust, G., Araç, D., Engel, F. B., Formstone, C. J., Fredriksson, R., Hall, R. A., Harty, B. L., Kirchhoff, C., Knapp, B., et al. (2015) · Pharmacological Reviews · doi:10.1124/pr.114.009647 · Cited by 489 · see citing works
Self-citationThe Wnt Pathway: From Signaling Mechanisms to Synthetic Modulators
Rim, E. Y., Clevers, H. C., & Nusse, R. (2022) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-040320-103615 · Cited by 488 · see citing works
Structure of the human smoothened receptor bound to an antitumour agent
Wang, C., Wu, H., Katritch, V., Han, G. W., Huang, X., Liu, W., Siu, F., Roth, B. L., Cherezov, V., & Stevens, R. C. (2013) · Nature · doi:10.1038/nature12167 · Cited by 465 · see citing works
Molecular Biology of Atherosclerosis
Hopkins, P. N. (2013) · Physiological Reviews · doi:10.1152/physrev.00004.2012 · Cited by 456 · see citing works
Molecular evolution of peptidergic signaling systems in bilaterians
Mirabeau, O., & Joly, J. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1219956110 · Cited by 423 · see citing works
Evolution of phototransduction, vertebrate photoreceptors and retina
Lamb, T. D. (2013) · Progress in Retinal and Eye Research · doi:10.1016/j.preteyeres.2013.06.001 · Cited by 387 · see citing works
Selectivity determinants of GPCR–G-protein binding
Flock, T., Hauser, A. S., Lund, N., Gloriam, D. E., Balaji, S., & Babu, M. M. (2017) · Nature · doi:10.1038/nature22070 · Cited by 384 · see citing works
Loh, K. M., van Amerongen, R., & Nusse, R. (2016) · Developmental Cell · doi:10.1016/j.devcel.2016.08.011 · Cited by 335 · see citing works
Heterotrimeric G protein signalling in the plant kingdom
Urano, D., Chen, J., Botella, J. R., & Jones, A. M. (2013) · Open Biology · doi:10.1098/rsob.120186 · Cited by 285 · see citing works
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Langenhan, T., Aust, G., & Hamann, J. (2013) · Science Signaling · doi:10.1126/scisignal.2003825 · Cited by 267 · see citing works
de Mendoza, A., Sebé-Pedrós, A., & Ruiz‐Trillo, I. (2014) · Genome Biology and Evolution · doi:10.1093/gbe/evu038 · Cited by 194 · see citing works
Mechanisms of adhesion G protein–coupled receptor activation
Vizurraga, A., Adhikari, R., Yeung, J., Yu, M., & Tall, G. G. (2020) · Journal of Biological Chemistry · doi:10.1074/jbc.rev120.007423 · Cited by 179 · see citing works
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López, S., Bermúdez, B., la Paz, S. M., Jaramillo, S., Varela, L. M., Ortega‐Gómez, A., Abia, R., & Muriana, F. J. G. (2014) · Biochimica et Biophysica Acta (BBA) - Biomembranes · doi:10.1016/j.bbamem.2014.01.007 · Cited by 166 · see citing works
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Frooninckx, L., Rompay, L. V., Temmerman, L., Sinay, E. V., Beets, I., Janssen, T. A. H., Husson, S. J., & Schoofs, L. (2012) · Frontiers in Endocrinology · doi:10.3389/fendo.2012.00167 · Cited by 161 · see citing works
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Prömel, S., Langenhan, T., & Araç, D. (2013) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2013.06.002 · Cited by 98 · see citing works
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Lipke, P. (2018) · Journal of Fungi · doi:10.3390/jof4020059 · Cited by 81 · see citing works
Cvicek, V., Goddard, W. A., & Abrol, R. (2016) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004805 · Cited by 92 · see citing works
Krishnan, A., & Schiöth, H. B. (2015) · Journal of Experimental Biology · doi:10.1242/jeb.110312 · Cited by 81 · see citing works
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Bradford, W. S., Buckholz, A. P., Morton, J., Price, C. M., Jones, A. M., & Urano, D. (2013) · Science Signaling · doi:10.1126/scisignal.2003768 · Cited by 77 · see citing works
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Sandal, M., Behrens, M., Brockhoff, A., Musiani, F., Giorgetti, A., Carloni, P., & Meyerhof, W. (2015) · Journal of Chemical Theory and Computation · doi:10.1021/acs.jctc.5b00472 · Cited by 73 · see citing works
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Mushegian, A. R., Gurevich, V. V., & Gurevich, E. V. (2012) · PLoS ONE · doi:10.1371/journal.pone.0033806 · Cited by 70 · see citing works
Glycoprotein Hormones and Their Receptors Emerged at the Origin of Metazoans
Roch, G. J., & Sherwood, N. M. (2014) · Genome Biology and Evolution · doi:10.1093/gbe/evu118 · Cited by 69 · see citing works
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Lin, H., Hsiao, C., Pabst, C., Hébert, J., Schöneberg, T., & Hamann, J. (2017) · Advances in immunology · doi:10.1016/bs.ai.2017.05.005 · Cited by 67 · see citing works
Peeters, M. C., Fokkelman, M., Boogaard, B., Egerod, K. L., van de Water, B., IJzerman, A. P., & Schwartz, T. W. (2015) · Cellular Signalling · doi:10.1016/j.cellsig.2015.08.015 · Cited by 67 · see citing works
Towards the Idea of Molecular Brains
Timsit, Y., & Sergeant-Perthuis, G. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms222111868 · Cited by 72 · see citing works
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Hwang, J., Moon, M. J., Park, S., Kim, D., Cho, E. B., Ha, N., Son, G. H., Kim, K., Vaudry, H., & Seong, J. Y. (2013) · Molecular Biology and Evolution · doi:10.1093/molbev/mst031 · Cited by 64 · see citing works
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Krishnan, A., Dnyansagar, R., Almén, M. S., Williams, M. J., Fredriksson, R., Manoj, N., & Schiöth, H. B. (2014) · BMC Evolutionary Biology · doi:10.1186/s12862-014-0270-4 · Cited by 54 · see citing works
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Katz, P. S., & Lillvis, J. L. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2014.05.002 · Cited by 50 · see citing works
Eukaryotic G protein-coupled receptors as descendants of prokaryotic sodium-translocating rhodopsins
Shalaeva, D. N., Galperin, M. Y., & Mulkidjanian, A. Y. (2015) · Biology Direct · doi:10.1186/s13062-015-0091-4 · Cited by 46 · see citing works
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Duc, D. L., Schulz, A., Lede, V., Schulze, A., Thor, D., Brüser, A., & Schöneberg, T. (2017) · Advances in immunology · doi:10.1016/bs.ai.2017.05.006 · Cited by 50 · see citing works
Martin, J. F., van den Berg, M. A., van Themaat, E. V. L., & Liras, P. (2019) · Biotechnology Advances · doi:10.1016/j.biotechadv.2019.04.014 · Cited by 50 · see citing works
Cabrera, I. E., Pacentine, I. V., Lim, A., Guerrero, N., Kryštofová, S., Li, L., Michkov, A. V., Servin, J. A., Ahrendt, S. R., Carrillo, A. J., et al. (2015) · G3 Genes Genomes Genetics · doi:10.1534/g3.115.020974 · Cited by 46 · see citing works
Evolutionary hierarchy of vertebrate-like heterotrimeric G protein families
Krishnan, A., Mustafa, A., Almén, M. S., Fredriksson, R., Williams, M. J., & Schiöth, H. B. (2015) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2015.05.009 · Cited by 46 · see citing works
Self-citationDissecting signaling and functions of adhesion G protein–coupled receptors
Araç, D., Aust, G., Calebiro, D., Engel, F. B., Formstone, C. J., Goffinet, A. M., Hamann, J., Kittel, R. J., Liebscher, I., Lin, H., et al. (2012) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.2012.06820.x · Cited by 45 · see citing works
Self-citationFeeding and the Rhodopsin Family G-Protein Coupled Receptors in Nematodes and Arthropods
Cardoso, J. C. R., Félix, R. C., Fonseca, V. G., & Power, D. M. (2012) · Frontiers in Endocrinology · doi:10.3389/fendo.2012.00157 · Cited by 42 · see citing works
Retracing the path of planar cell polarity
Schenkelaars, Q., Fierro‐Constaín, L., Renard, E., & Borchiellini, C. (2016) · BMC Evolutionary Biology · doi:10.1186/s12862-016-0641-0 · Cited by 40 · see citing works
Prevertebrate Local Gene Duplication Facilitated Expansion of the Neuropeptide GPCR Superfamily
Yun, S., Furlong, M., Sim, M., Cho, M., Park, S., Cho, E. B., Reyes‐Alcaraz, A., Hwang, J., Kim, J., & Seong, J. Y. (2015) · Molecular Biology and Evolution · doi:10.1093/molbev/msv179 · Cited by 41 · see citing works
Bondarev, A. D., Attwood, M. M., Jonsson, J., Chubarev, V. N., Tarasov, V. V., & Schiöth, H. B. (2020) · Expert Opinion on Drug Discovery · doi:10.1080/17460441.2020.1791075 · Cited by 40 · see citing works
Self-citationConvergent evolution of animal and microbial rhodopsins
Kojima, K., & Sudo, Y. (2023) · RSC Advances · doi:10.1039/d2ra07073a · Cited by 40 · see citing works
The nervous system of Xenacoelomorpha: a genomic perspective
Perea-Atienza, E., Gavilán, B., Chiodin, M., Abril, J. F., Hoff, K. J., Poustka, A. J., & Martı́nez, P. (2015) · Journal of Experimental Biology · doi:10.1242/jeb.110379 · Cited by 39 · see citing works
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Jean-Charles, P.-Y., Snyder, J. C., & Shenoy, S. K. (2016) · Progress in molecular biology and translational science · doi:10.1016/bs.pmbts.2016.05.001 · Cited by 39 · see citing works
Hahnel, S. R., Wheeler, N. J., Lu, Z., Wangwiwatsin, A., McVeigh, P., Maule, A. G., Berriman, M., Day, T. A., Ribeiro, P., & Grevelding, C. G. (2018) · PLoS Pathogens · doi:10.1371/journal.ppat.1006718 · Cited by 38 · see citing works
Whole Genome Wide Expression Profiles on Germination of Verticillium dahliae Microsclerotia
Hu, D., Wang, C., Tao, F., Cui, Q., Xu, X., Shang, W., & Hu, X. (2014) · PLoS ONE · doi:10.1371/journal.pone.0100046 · Cited by 38 · see citing works
Krishnan, A., Almén, M. S., Fredriksson, R., & Schiöth, H. B. (2013) · Gene · doi:10.1016/j.gene.2013.05.005 · Cited by 36 · see citing works
Self-citationViriyakosol, S., Singhania, A., Fierer, J., Goldberg, J. M., Kirkland, T. N., & Woelk, C. H. (2013) · BMC Microbiology · doi:10.1186/1471-2180-13-121 · Cited by 38 · see citing works
Vibrational resonance, allostery, and activation in rhodopsin-like G protein-coupled receptors
Woods, K. N., Pfeffer, J., Dutta, A., & Klein‐Seetharaman, J. (2016) · Scientific Reports · doi:10.1038/srep37290 · Cited by 32 · see citing works
Computational studies to predict or explain G protein coupled receptor polypharmacology
Jacobson, K. A., Costanzi, S., & Paoletta, S. (2014) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2014.10.009 · Cited by 31 · see citing works
Daddam, J. R., Sreenivasulu, B., Peddanna, K., & Katike, U. (2020) · RSC Advances · doi:10.1039/c9ra09245e · Cited by 30 · see citing works
New functions and signaling mechanisms for the class of adhesion G protein–coupled receptors
Liebscher, I., Ackley, B. D., Araç, D., Ariestanti, D. M., Aust, G., Bae, B.-I., Bista, B. R., Bridges, J. P., Duman, J. G., Engel, F. B., et al. (2014) · Annals of the New York Academy of Sciences · doi:10.1111/nyas.12580 · Cited by 30 · see citing works
Self-citationHow to bake a brain: yeast as a model neuron
Sarto‐Jackson, I., & Tomáška, Ľ. (2016) · Current Genetics · doi:10.1007/s00294-015-0554-2 · Cited by 28 · see citing works
The evolutionary analysis reveals domain fusion of proteins with Frizzled-like CRD domain
Yan, J., Jia, H., Ma, Z., Ye, H., Zhou, M., Su, L., Liu, J., & Guo, A. (2013) · Gene · doi:10.1016/j.gene.2013.09.083 · Cited by 27 · see citing works
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Peraza‐Reyes, L., Brun, S., Grognet, P., & Malagnac, F. (2016) · The mycota · doi:10.1007/978-3-032-15548-1_13 · Cited by 27 · see citing works
Plattner, H. (2015) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12218 · Cited by 26 · see citing works
Seppälä, S., Solomon, K., Gilmore, S. P., Henske, J. K., & O’Malley, M. (2016) · Microbial Cell Factories · doi:10.1186/s12934-016-0611-7 · Cited by 25 · see citing works
Effect of nitroprusside on arteriolar constriction after retinal branch vein occlusion.
Donati, G., Pournaras, C. J., & Tsacopoulos, M. (1998) · PubMed · Cited by 26 · see citing works
Alzugaray, M. E., Bruno, M. C., Sambucaro, M. J. V., & Ronderos, J. R. (2019) · Scientific Reports · doi:10.1038/s41598-019-46712-9 · Cited by 25 · see citing works
Gao, J., Xu, X., Huang, K.-L., & Liang, Z.-H. (2021) · Frontiers in Microbiology · doi:10.3389/fmicb.2021.631392 · Cited by 29 · see citing works
Mickael, M., Rajput, A. B., Steyn, J. S., Wiemerslage, L., & Bürglin, T. R. (2016) · Comparative Biochemistry and Physiology Part D Genomics and Proteomics · doi:10.1016/j.cbd.2016.08.005 · Cited by 24 · see citing works
Comprehensive, structurally-informed alignment and phylogeny of vertebrate biogenic amine receptors
Spielman, S., Kumar, K., & Wilke, C. (2015) · PeerJ · doi:10.7717/peerj.773 · Cited by 19 · see citing works
Dynamics and mechanistic underpinnings to pharmacology of class A GPCRs: an NMR perspective
Huang, S. K., & Prosser, R. S. (2022) · American Journal of Physiology-Cell Physiology · doi:10.1152/ajpcell.00044.2022 · Cited by 22 · see citing works
A brief review on the evolution of GPCR: conservation and diversification
Zhang, Z., Wu, J., Yu, J. M., & Xiao, J. (2012) · Open Journal of Genetics · doi:10.4236/ojgen.2012.24b003 · Cited by 22 · see citing works
Powell, M. J. (2017) · Springer eBooks · doi:10.1007/978-3-319-28149-0_17 · Cited by 22 · see citing works
Ren, J., Chung‐Davidson, Y., Jia, L., & Li, W. (2019) · BMC Evolutionary Biology · doi:10.1186/s12862-019-1463-7 · Cited by 21 · see citing works
Mojib, N., & Kubanek, J. (2019) · Limnology and Oceanography · doi:10.1002/lno.11345 · Cited by 20 · see citing works
HTR6 and SSTR3 targeting to primary cilia
Barbeito, P., & Garcia-Gonzalo, F. R. (2021) · Biochemical Society Transactions · doi:10.1042/bst20191005 · Cited by 20 · see citing works
An Ancient Autoproteolytic Domain Found in GAIN, ZU5 and Nucleoporin98
Liao, Y., Pei, J., Cheng, H., & Grishin, N. V. (2014) · Journal of Molecular Biology · doi:10.1016/j.jmb.2014.10.011 · Cited by 20 · see citing works
Kerekes, K., Bányai, L., Trexler, M., & Patthy, L. (2019) · Growth Factors · doi:10.1080/08977194.2019.1626380 · Cited by 20 · see citing works
Rump, M. T., Kozma, M. T., Pawar, S., & Derby, C. D. (2021) · PLoS ONE · doi:10.1371/journal.pone.0252066 · Cited by 20 · see citing works
Bendena, W. G., Campbell, J. C., Zara, L. C., Tobe, S. S., & Chin-Sang, I. D. (2012) · Frontiers in Endocrinology · doi:10.3389/fendo.2012.00093 · Cited by 19 · see citing works
The Role of Neuropeptide-Stimulated cAMP-EPACs Signalling in Cancer Cells
Gao, Z., Lei, W. I., & Lee, L. T. O. (2022) · Molecules · doi:10.3390/molecules27010311 · Cited by 18 · see citing works
Peeters, M. C., Mos, I., Lenselink, E. B., Lucchesi, M., IJzerman, A. P., & Schwartz, T. W. (2016) · The FASEB Journal · doi:10.1096/fj.201500110 · Cited by 18 · see citing works
Cartography of rhodopsin-like G protein-coupled receptors across vertebrate genomes
Rinne, M. K., Tanoli, Z.-U.-R., Khan, A., & Xhaard, H. (2019) · Scientific Reports · doi:10.1038/s41598-018-33120-8 · Cited by 15 · see citing works
Modulating vertebrate physiology by genomic fine-tuning of GPCR functions
Schöneberg, T. (2024) · Physiological Reviews · doi:10.1152/physrev.00017.2024 · Cited by 17 · see citing works
The Relevance of Genomic Signatures at Adhesion GPCR Loci in Humans
Kovacs, P. L., & Schöneberg, T. (2016) · Handbook of experimental pharmacology · doi:10.1007/978-3-319-41523-9_9 · Cited by 17 · see citing works
G-protein-coupled Receptors in Fungi
El-Defrawy, M. M. H., & Hesham, A. E. (2020) · Fungal biology · doi:10.1007/978-3-030-41870-0_3 · Cited by 18 · see citing works
Photoreceptors mapping from past history till date
Parihar, P., Singh, R., Singh, S., Tripathi, D. K., Chauhan, D. K., Singh, V. P., & Prasad, S. M. (2016) · Journal of Photochemistry and Photobiology B Biology · doi:10.1016/j.jphotobiol.2016.06.020 · Cited by 17 · see citing works
Highly diversified expansions shaped the evolution of membrane bound proteins in metazoans
Attwood, M. M., Krishnan, A., Almén, M. S., & Schiöth, H. B. (2017) · Scientific Reports · doi:10.1038/s41598-017-11543-z · Cited by 14 · see citing works
Self-citationGu, X., Chen, Z., & Wang, D. (2020) · Frontiers in Bioengineering and Biotechnology · doi:10.3389/fbioe.2020.00635 · Cited by 15 · see citing works
Kim, D., Park, J. C., & Lee, J. (2022) · Comparative Biochemistry and Physiology Part C Toxicology & Pharmacology · doi:10.1016/j.cbpc.2022.109297 · Cited by 15 · see citing works
- Authors
- Krishnan, A., Almén, M. S., Fredriksson, R., & Schiöth, H. B.
- Affiliations
- Uppsala University (SE)
- Corresponding author
- Schiöth, Helgi B.
- Venue
- PLoS ONE
- Publisher
- Public Library of Science (PLoS)
- Published
- 2012-01-04
- Volume
- 7
- Issue
- 1
- Pages
- e29817
- ISSN
- 1932-6203 (ISSN-L)
- PMC
- PMC3251606
- OpenAlex
- W1983820999
- Cited by
- 204
- References
- 47
- Citations by year
- 2026: 6 · 2025: 11 · 2024: 16 · 2023: 11 · 2022: 11 · 2021: 7 · 2020: 16 · 2019: 14 · 2018: 8 · 2017: 14 · 2016: 23 · 2015: 20 · 2014: 18 · 2013: 18 · 2012: 10
- FWCI
- 8.48
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- PLoS ONE (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Uppsala University Publications (Uppsala University) (submittedVersion, other-oa)
- RePEc: Research Papers in Economics (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Figshare (submittedVersion, cc-by)
- Funders
- Novo Nordisk
- Vetenskapsrådet
- Magnus Bergvalls Stiftelse
- Uppsala Universitet
- Novo Nordisk Fonden
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Receptor Mechanisms and Signaling
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Fungal and yeast genetics research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- G protein-coupled receptors, GPCR evolution, rhodopsin family, cell adhesion receptors, glutamate receptors, Frizzled receptors, N-terminal domain, Salpingoeca rosetta, Capsaspora owczarzaki, Blastocladiomycota, Chytridiomycota, fungal genome
- MeSH terms
- Amino Acid Sequence, Animals, Cloning, Molecular, Fungi, Genes, Fungal, Humans, Mammals, Molecular Sequence Data, Phylogeny, Rhodopsin, Cell Adhesion Molecules, Genome, Fungal, Receptors, Glutamate, Evolution, Molecular, Receptors, G-Protein-Coupled, Frizzled Receptors
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