A family of non-GPCR chemosensors defines an alternative logic for mammalian olfaction
Open accessAbstract
Odor perception in mammals is mediated by parallel sensory pathways that convey distinct information about the olfactory world. Multiple olfactory subsystems express characteristic seven-transmembrane G-protein-coupled receptors (GPCRs) in a one-receptor-per-neuron pattern that facilitates odor discrimination. Sensory neurons of the "necklace" subsystem are nestled within the recesses of the olfactory epithelium and detect diverse odorants; however, they do not express known GPCR odor receptors. Here, we report that members of the four-pass transmembrane MS4A protein family are chemosensors expressed within necklace sensory neurons. These receptors localize to sensory endings and confer responses to ethologically relevant ligands, including pheromones and fatty acids, in vitro and in vivo. Individual necklace neurons co-express many MS4A proteins and are activated by multiple MS4A ligands; this pooling of information suggests that the necklace is organized more like subsystems for taste than for smell. The MS4As therefore define a distinct mechanism and functional logic for mammalian olfaction.
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?
Cells exposed to CD200 and CX3CL1 responded differentially to fAβ, increasing expression of genes involved in neuronal cell surface motif recognition or phagocytosis of CNS substrates, including MS4A genes, TREM2, TYROBP, CD33, and ABCA7.
“Whereas cells exposed to these two factors responded differentially to fAβ, increasing expression of genes involved in neuronal cell surface motif recognition, or phagocytosis of CNS substrates, including MS4A genes, TREM2, TYROBP, CD33, and ABCA7 (Bradshaw et al., 2013; Fu et al., 2016; Greer et al., 2016)(Figure S6B).”
From iPSC-derived human microglia-like cells to study neurological diseases (2017) · cites this paper as Greer et al., 2016
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
A novel multigene family may encode odorant receptors: A molecular basis for odor recognition
Buck, L., & Axel, R. (1991) · Cell · doi:10.1016/0092-8674(91)90418-x · Cited by 4,987 · see citing works
(2012) · doi:10.1016/j.jmoldx.2011.08.002 · Cited by 2,567 · see citing works
A Novel Family of Mammalian Taste Receptors
Adler, E., Hoon, M. A., Mueller, K. L., Chandrashekar, J. V., Ryba, N. J. P., & Zuker, C. S. (2000) · Cell · doi:10.1016/s0092-8674(00)80705-9 · Cited by 1,360 · see citing works
Variant Ionotropic Glutamate Receptors as Chemosensory Receptors in Drosophila
Benton, R., Vannice, K., Gomez‐Diaz, C., & Vosshall, L. B. (2009) · Cell · doi:10.1016/j.cell.2008.12.001 · Cited by 1,320 · see citing works
A novel family of genes encoding putative pheromone receptors in mammals
Dulac, C., & Axel, R. (1995) · Cell · doi:10.1016/0092-8674(95)90161-2 · Cited by 1,001 · see citing works
A second class of chemosensory receptors in the olfactory epithelium
Liberles, S. D., & Buck, L. B. (2006) · Nature · doi:10.1038/nature05066 · Cited by 791 · see citing works
Trp ion channels and temperature sensation
Dhaka, A., Viswanath, V., & Patapoutian, A. (2006) · Annual Review of Neuroscience · doi:10.1146/annurev.neuro.29.051605.112958 · Cited by 782 · see citing works
A Multigene Family Encoding a Diverse Array of Putative Pheromone Receptors in Mammals
Matsunami, H., & Buck, L. B. (1997) · Cell · doi:10.1016/s0092-8674(00)80537-1 · Cited by 706 · see citing works
Herrada, G., & Dulac, C. (1997) · Cell · doi:10.1016/s0092-8674(00)80536-x · Cited by 696 · see citing works
Divergent seven transmembrane receptors are candidate chemosensory receptors in C. elegans
Troemel, E. R., Chou, J. H., Dwyer, N. D., Colbert, H. A., & Bargmann, C. I. (1995) · Cell · doi:10.1016/0092-8674(95)90162-0 · Cited by 684 · see citing works
Terakita, A. (2005) · Genome biology · doi:10.1186/gb-2005-6-3-213 · Cited by 632 · see citing works
The evolution of animal chemosensory receptor gene repertoires: roles of chance and necessity
Nei, M., Niimura, Y., & Nozawa, M. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2480 · Cited by 626 · see citing works
A New Multigene Family of Putative Pheromone Receptors
Ryba, N. J. P., & Tirindelli, R. (1997) · Neuron · doi:10.1016/s0896-6273(00)80946-0 · Cited by 598 · see citing works
Functional Architecture of Olfactory Ionotropic Glutamate Receptors
Abuin, L., Bargeton, B., Ulbrich, M. H., Isacoff, E. Y., Kellenberger, S., & Benton, R. (2011) · Neuron · doi:10.1016/j.neuron.2010.11.042 · Cited by 580 · see citing works
Odor Coding by a Mammalian Receptor Repertoire
Saito, H., Chi, Q., Zhuang, H., Matsunami, H., & Mainland, J. D. (2009) · Science Signaling · doi:10.1126/scisignal.2000016 · Cited by 563 · see citing works
Transient receptor potential ion channels as participants in thermosensation and thermoregulation
Caterina, M. J. (2006) · American Journal of Physiology-Regulatory, Integrative and Comparative Physiology · doi:10.1152/ajpregu.00446.2006 · Cited by 442 · see citing works
Formyl peptide receptor-like proteins are a novel family of vomeronasal chemosensors
Rivière, S., Challet, L., Fluegge, D., Spehr, M., & Rodríguez, I. (2009) · Nature · doi:10.1038/nature08029 · Cited by 383 · see citing works
The FcεRIβ Subunit Functions as an Amplifier of FcεRIγ-Mediated Cell Activation Signals
Lin, S., Cicala, C., Scharenberg, A. M., & Kinet, J.-P. (1996) · Cell · doi:10.1016/s0092-8674(00)81300-8 · Cited by 355 · see citing works
Bubien, J. K., Zhou, L. J., Bell, P. D., Frizzell, R. A., & Tedder, T. F. (1993) · The Journal of Cell Biology · doi:10.1083/jcb.121.5.1121 · Cited by 354 · see citing works
How Is the Olfactory Map Formed and Interpreted in the Mammalian Brain?
Mori, K., & Sakano, H. (2011) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-112210-112917 · Cited by 350 · see citing works
Subsystem Organization of the Mammalian Sense of Smell
Munger, S. D., Leinders‐Zufall, T., & Zufall, F. (2008) · Annual Review of Physiology · doi:10.1146/annurev.physiol.70.113006.100608 · Cited by 317 · see citing works
Molecular organization of vomeronasal chemoreception
Isogai, Y., Si, S., Pont-Lezica, L., Tan, T., Kapoor, V., Murthy, V. N., & Dulac, C. (2011) · Nature · doi:10.1038/nature10437 · Cited by 317 · see citing works
Axel, R. (1995) · Scientific American · doi:10.1038/scientificamerican1095-154 · Cited by 314 · see citing works
Juilfs, D. M., Fülle, H., Zhao, A. Z., Houslay, M. D., Garbers, D. L., & Beavo, J. A. (1997) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.94.7.3388 · Cited by 310 · see citing works
A receptor guanylyl cyclase expressed specifically in olfactory sensory neurons.
Fülle, H., Vassar, R. J., Foster, D. C., Yang, R., Axel, R., & Garbers, D. L. (1995) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.92.8.3571 · Cited by 271 · see citing works
Evolutionary deterioration of the vomeronasal pheromone transduction pathway in catarrhine primates
Zhang, J., & Webb, D. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1331721100 · Cited by 258 · see citing works
Formyl peptide receptors are candidate chemosensory receptors in the vomeronasal organ
Liberles, S. D., Horowitz, L. F., Kuang, D., Contos, J. J. A., Wilson, K. L., Siltberg-Liberles, J., Liberles, D. A., & Buck, L. B. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0904464106 · Cited by 246 · see citing works
Detection of Near-Atmospheric Concentrations of CO 2 by an Olfactory Subsystem in the Mouse
Hu, J., Zhong, C., Cheng, D., Chi, Q., Walz, A., Mombaerts, P., Matsunami, H., & Luo, M. (2007) · Science · doi:10.1126/science.1144233 · Cited by 235 · see citing works
G Protein-Coupled Receptors in Human Fat Taste Perception
Galindo, M. M., Voigt, N., Stein, J., van Lengerich, J., Raguse, J. D., Hofmann, T. F., Meyerhof, W., & Behrens, M. (2011) · Chemical Senses · doi:10.1093/chemse/bjr069 · Cited by 229 · see citing works
Leinders‐Zufall, T., Cockerham, R. E., Michalakis, S., Biel, M., Garbers, D. L., Reed, R. R., Zufall, F., & Munger, S. D. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0704965104 · Cited by 228 · see citing works
Allergy-Associated FcRβ Is a Molecular Amplifier of IgE- and IgG-Mediated In Vivo Responses
Dombrowicz, D., Lin, S., Flamand, V., Brini, A. T., Koller, B. H., & Kinet, J.-P. (1998) · Immunity · doi:10.1016/s1074-7613(00)80556-7 · Cited by 208 · see citing works
Co-Expression of Putative Pheromone Receptors in the Sensory Neurons of the Vomeronasal Organ
Martini, S., Silvotti, L., Shirazi, A., Ryba, N. J. P., & Tirindelli, R. (2001) · Journal of Neuroscience · doi:10.1523/jneurosci.21-03-00843.2001 · Cited by 191 · see citing works
Odorant Receptors on Axon Termini in the Brain
Barnea, G., O'Donnell, S., Mancia, F., Sun, X., Nemes, A., Mendelsohn, M. M., & Axel, R. (2004) · Science · doi:10.1126/science.1096146 · Cited by 181 · see citing works
An Olfactory Subsystem that Detects Carbon Disulfide and Mediates Food-Related Social Learning
Munger, S. D., Leinders‐Zufall, T., McDougall, L. M., Cockerham, R. E., Schmid, A., Wandernoth, P. M., Wennemuth, G., Biel, M., Zufall, F., & Kelliher, K. R. (2010) · Current Biology · doi:10.1016/j.cub.2010.06.021 · Cited by 176 · see citing works
A cGMP-signaling pathway in a subset of olfactory sensory neurons
Meyer, M. R., Angele, A., Kremmer, E., Kaupp, U. B., & Müller, F. U. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.19.10595 · Cited by 172 · see citing works
Janas, E., Priest, R. C., Wilde, J. I., White, J. H., & Malhotra, R. (2005) · Clinical & Experimental Immunology · doi:10.1111/j.1365-2249.2005.02720.x · Cited by 162 · see citing works
Human olfactory receptor responses to odorants
Mainland, J. D., Li, Y. R., Zhou, T., Liu, W. L. L., & Matsunami, H. (2015) · Scientific Data · doi:10.1038/sdata.2015.2 · Cited by 158 · see citing works
Prediction of the odorant binding site of olfactory receptor proteins by human–mouse comparisons
Man, O., Gilad, Y., & Lancet, D. (2003) · Protein Science · doi:10.1110/ps.03296404 · Cited by 155 · see citing works
Hirota, J., & Mombaerts, P. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0400940101 · Cited by 152 · see citing works
CD20 Homo-oligomers Physically Associate with the B Cell Antigen Receptor
Polyak, M. J., Li, H., Shariat, N., & Deans, J. P. (2008) · Journal of Biological Chemistry · doi:10.1074/jbc.m800784200 · Cited by 147 · see citing works
Regulation of the Probability of Mouse Odorant Receptor Gene Choice
Khan, M., Vaes, E., & Mombaerts, P. (2011) · Cell · doi:10.1016/j.cell.2011.09.049 · Cited by 141 · see citing works
Molecular profiling of activated olfactory neurons identifies odorant receptors for odors in vivo
Jiang, Y., Gong, N. N., Hu, X. S., Ni, M. J., Pasi, R., & Matsunami, H. (2015) · Nature Neuroscience · doi:10.1038/nn.4104 · Cited by 133 · see citing works
The MS4A family: counting past 1, 2 and 3
Kuek, L. E., Leffler, M., Mackay, G. A., & Hulett, M. D. (2015) · Immunology and Cell Biology · doi:10.1038/icb.2015.48 · Cited by 126 · see citing works
Guanylyl cyclase-D in the olfactory CO 2 neurons is activated by bicarbonate
Sun, L., Wang, H., Hu, J., Han, J., Matsunami, H., & Luo, M. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0812220106 · Cited by 120 · see citing works
Grus, W. E., & Zhang, J. (2008) · Molecular Biology and Evolution · doi:10.1093/molbev/msn262 · Cited by 114 · see citing works
“Necklace olfactory glomeruli” form unique components of the rat primary olfactory system
Shinoda, K., Shiotani, Y., & Osawa, Y. (1989) · The Journal of Comparative Neurology · doi:10.1002/cne.902840304 · Cited by 108 · see citing works
Ionotropic and metabotropic mechanisms in chemoreception: 'chance or design'?
Silbering, A. F., & Benton, R. (2010) · EMBO Reports · doi:10.1038/embor.2010.8 · Cited by 103 · see citing works
Analysis of the Molecular Basis for Octanal Interactions in the Expressed Rat I7 Olfactory Receptor
Singer, M. S. (2000) · Chemical Senses · doi:10.1093/chemse/25.2.155 · Cited by 96 · see citing works
Sabir, A. A., Unver, A., & Kara, Z. (2012) · Journal of the Science of Food and Agriculture · doi:10.1002/jsfa.5571 · Cited by 92 · see citing works
Hayakawa, T., Suzuki–Hashido, N., Matsui, A., & Go, Y. (2014) · Molecular Biology and Evolution · doi:10.1093/molbev/msu144 · Cited by 76 · see citing works
MS4A12 Is a Colon-Selective Store-Operated Calcium Channel Promoting Malignant Cell Processes
Koslowski, M., Şahin, U., Dhaene, K., Huber, C., & Türeci, Ö. (2008) · Cancer Research · doi:10.1158/0008-5472.can-07-5768 · Cited by 73 · see citing works
Howie, D., Nolan, K. F., Daley, S. R., Butterfield, E., Adams, E., Rueda, H. G., Thompson, C., Saunders, N. J. S. G., Cobbold, S. P., Tone, Y., et al. (2009) · The Journal of Immunology · doi:10.4049/jimmunol.0901070 · Cited by 72 · see citing works
Chemosensory Receptor Specificity and Regulation
Dalton, R. P., & Lomvardas, S. (2015) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-071714-034145 · Cited by 72 · see citing works
Phylogenetic Analysis of the MS4A and TMEM176 Gene Families
Zuccolo, J., Bau, J. A., Childs, S. J., Goss, G. G., Sensen, C. W., & Deans, J. P. (2010) · PLoS ONE · doi:10.1371/journal.pone.0009369 · Cited by 71 · see citing works
Chemosensory signals and their receptors in the olfactory neural system
Ihara, S., Yoshikawa, K., & Touhara, K. (2013) · Neuroscience · doi:10.1016/j.neuroscience.2013.08.063 · Cited by 70 · see citing works
Molecular Biophysics of Orai Store-Operated Ca2+ Channels
Amcheslavsky, A., Wood, M. L., Yeromin, A. V., Parker, I., Freites, J. A., Tobias, D. J., & Cahalan, M. D. (2015) · Biophysical Journal · doi:10.1016/j.bpj.2014.11.3473 · Cited by 69 · see citing works
ONE-GC membrane guanylate cyclase, a trimodal odorant signal transducer
Duda, T., & Sharma, R. K. (2008) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2007.12.153 · Cited by 62 · see citing works
A Critical Period Defined by Axon-Targeting Mechanisms in the Murine Olfactory Bulb
Tsai, L., & Barnea, G. (2014) · Science · doi:10.1126/science.1248806 · Cited by 59 · see citing works
Stimulation of Guanylyl Cyclase-D by Bicarbonate
Guo, D., Zhang, J. J., & Huang, X. (2009) · Biochemistry · doi:10.1021/bi900441v · Cited by 57 · see citing works
Degeneration of the Olfactory Guanylyl Cyclase D Gene during Primate Evolution
Young, J. M., Waters, H. N., Dong, C., Fülle, H., & Liman, E. R. (2007) · PLoS ONE · doi:10.1371/journal.pone.0000884 · Cited by 54 · see citing works
Secundo, L., Snitz, K., & Sobel, N. (2014) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2013.12.010 · Cited by 50 · see citing works
Grueneberg Ganglion Neurons Are Activated by a Defined Set of Odorants
Mamasuew, K., Hofmann, N., Breer, H., & Fleischer, J. (2010) · Chemical Senses · doi:10.1093/chemse/bjq124 · Cited by 50 · see citing works
Cruse, G., Beaven, M. A., Ashmole, I., Bradding, P. H., Gilfillan, A. M., & Metcalfe, D. D. (2013) · Immunity · doi:10.1016/j.immuni.2013.04.007 · Cited by 47 · see citing works
Arakawa, H., Kelliher, K. R., Zufall, F., & Munger, S. D. (2013) · Chemical Senses · doi:10.1093/chemse/bjt015 · Cited by 46 · see citing works
CD36 is involved in oleic acid detection by the murine olfactory system
Oberland, S., Ackels, T., Gaab, S., Pelz, T., Spehr, J., Spehr, M., & Neuhaus, E. M. (2015) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2015.00366 · Cited by 43 · see citing works
Multimodal stimulus coding by a gustatory sensory neuron in Drosophila larvae
van Giesen, L., Hernandez-Nunez, L., Delasoie-Baranek, S., Colombo, M., Renaud, P., Bruggmann, R., Benton, R., Samuel, A. D. T., & Sprecher, S. G. (2016) · Nature Communications · doi:10.1038/ncomms10687 · Cited by 42 · see citing works
Cockerham, R. E., Puché, A. C., & Munger, S. D. (2009) · PLoS ONE · doi:10.1371/journal.pone.0004657 · Cited by 32 · see citing works
Signatures of Natural Selection in a Primate Bitter Taste Receptor
Wooding, S. (2011) · Journal of Molecular Evolution · doi:10.1007/s00239-011-9481-0 · Cited by 29 · see citing works
Kim, S. T., Do, I., Lee, J., Sohn, I., Kim, K.-M., & Kang, W. K. (2014) · Clinical & Translational Oncology · doi:10.1007/s12094-014-1258-7 · Cited by 15 · see citing works
Integration of CO2 and odorant signals in the mouse olfactory bulb
Gao, L., Hu, J., Zhong, C., & Luo, M. (2010) · Neuroscience · doi:10.1016/j.neuroscience.2010.08.006 · Cited by 9 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- van Giesen L Hernandez-Nunez L Delasoie-Baranek S Colombo M Renaud P Bruggmann R Benton R Samuel AD Sprecher SG Multimodal stimulus coding by a gustatory sensory neuron in Drosophila larvae. Nat Commun 2016 7 10687 26864722 PMC4753250
Cited by
Sorted by citations
Hammond, T. R., Dufort, C., Dissing-Olesen, L., Giera, S., Young, A., Wysoker, A., Walker, A. J., Segel, M., Nemesh, J., Saunders, A., et al. (2018) · doi:10.1101/406140 · Cited by 2,225 · see citing works
iPSC-derived human microglia-like cells to study neurological diseases
Abud, E. M., Ramirez, R. N., Martinez, E. S., Healy, L. M., Nguyen, C. H. H., Newman, S. A., Yeromin, A. V., Scarfone, V. M., Marsh, S. E., Fimbres, C., et al. (2017) · Neuron · doi:10.1016/j.neuron.2017.03.042 · Cited by 1,154 · see citing works
Late onset Alzheimer’s disease genetics implicates microglial pathways in disease risk
Efthymiou, A. G., & Goate, A. M. (2017) · Molecular Neurodegeneration · doi:10.1186/s13024-017-0184-x · Cited by 562 · see citing works
Non-canonical odor coding in the mosquito
Herre, M., Goldman, O. V., Lu, T., Caballero-Vidal, G., Qi, Y., Gilbert, Z. N., Gong, Z., Morita, T., Rahiel, S., Ghaninia, M., et al. (2022) · Cell · doi:10.1016/j.cell.2022.07.024 · Cited by 215 · see citing works
Sharma, A., Kumar, R., Aier, I., Semwal, R., Tyagi, P. K., & Varadwaj, P. K. (2018) · Current Neuropharmacology · doi:10.2174/1570159x17666181206095626 · Cited by 138 · see citing works
The Evolving Neural and Genetic Architecture of Vertebrate Olfaction
Bear, D. M., Lassance, J., Hoekstra, H. E., & Datta, S. R. (2016) · Current Biology · doi:10.1016/j.cub.2016.09.011 · Cited by 133 · see citing works
Mattiola, I., Tomay, F., Pizzol, M. D., Silva-Gomes, R., Savino, B., Gulić, T., Doni, A., Lonardi, S., Boutet, M., Nerviani, A., et al. (2019) · Nature Immunology · doi:10.1038/s41590-019-0417-y · Cited by 137 · see citing works
VSIG4 mediates transcriptional inhibition of Nlrp3 and Il-1 β in macrophages
Huang, X., Feng, Z., Jiang, Y., Li, J., Xiang, Q., Guo, S. J., Yang, C., Fei, L., Guo, G., Zheng, L., et al. (2019) · Science Advances · doi:10.1126/sciadv.aau7426 · Cited by 115 · see citing works
Signal Detection and Coding in the Accessory Olfactory System
Mohrhardt, J., Nagel, M., Fleck, D., Ben‐Shaul, Y., & Spehr, M. (2018) · Chemical Senses · doi:10.1093/chemse/bjy061 · Cited by 114 · see citing works
Microglial efferocytosis: Diving into the Alzheimer’s disease gene pool
Romero-Molina, C., Garretti, F., Andrews, S. J., Marcora, E., & Goate, A. M. (2022) · Neuron · doi:10.1016/j.neuron.2022.10.015 · Cited by 111 · see citing works
The tetraspan MS4A family in homeostasis, immunity, and disease
Mattiola, I., Mantovani, A., & Locati, M. (2021) · Trends in Immunology · doi:10.1016/j.it.2021.07.002 · Cited by 101 · see citing works
MS4A4A: a novel cell surface marker for M2 macrophages and plasma cells
Sanyal, R., Polyak, M. J., Zuccolo, J., Puri, M., Deng, L., Roberts, L., Zuba, A., Storek, J., Luider, J. M., Sundberg, E. M., et al. (2017) · Immunology and Cell Biology · doi:10.1038/icb.2017.18 · Cited by 99 · see citing works
Structural basis of amine odorant perception by a mammal olfactory receptor
Guo, L., Cheng, J., Lian, S., Liu, Q., Lü, Y., Zheng, Y., Zhu, K., Zhang, M., Kong, Y., Zhang, C., et al. (2023) · Nature · doi:10.1038/s41586-023-06106-4 · Cited by 98 · see citing works
Saraiva, L. R., Riveros-McKay, F., Mezzavilla, M., Abou-Moussa, E. H., Arayata, C. J., Makhlouf, M., Trimmer, C., Ibarra-Soria, X., Khan, M., Van Gerven, L., et al. (2019) · Science Advances · doi:10.1126/sciadv.aax0396 · Cited by 92 · see citing works
Shifting paradigms: The central role of microglia in Alzheimer’s disease
Schwabe, T., Srinivasan, K., & Rhinn, H. (2020) · Neurobiology of Disease · doi:10.1016/j.nbd.2020.104962 · Cited by 84 · see citing works
Principles of odor coding in vertebrates and artificial chemosensory systems
Manzini, I., Schild, D., & Natale, C. D. (2021) · Physiological Reviews · doi:10.1152/physrev.00036.2020 · Cited by 84 · see citing works
Odor coding in the mammalian olfactory epithelium
Kurian, S. M., Naressi, R. G., Manoel, D., Barwich, A., Malnic, B., & Saraiva, L. R. (2021) · Cell and Tissue Research · doi:10.1007/s00441-020-03327-1 · Cited by 78 · see citing works
The evolutionary origins of the vertebrate olfactory system
Poncelet, G., & Shimeld, S. M. (2020) · Open Biology · doi:10.1098/rsob.200330 · Cited by 69 · see citing works
Oteíza, P., & Baldwin, M. W. (2021) · Current Opinion in Neurobiology · doi:10.1016/j.conb.2021.08.005 · Cited by 74 · see citing works
Evolutionary ecology of chemosensation and its role in sensory drive
Yohe, L., & Brand, P. (2018) · Current Zoology · doi:10.1093/cz/zoy048 · Cited by 58 · see citing works
Kozma, M. T., Ngo-Vu, H., Wong, Y. Y., Shukla, N. S., Pawar, S., Senatore, A., Schmidt, M., & Derby, C. D. (2020) · PLoS ONE · doi:10.1371/journal.pone.0230266 · Cited by 64 · see citing works
Glezer, I., & Malnic, B. (2019) · Handbook of clinical neurology · doi:10.1016/b978-0-444-63855-7.00005-8 · Cited by 63 · see citing works
A Near-Complete Spatial Map of Olfactory Receptors in the Mouse Main Olfactory Epithelium
Tan, L., & Xie, X. S. (2018) · Chemical Senses · doi:10.1093/chemse/bjy030 · Cited by 59 · see citing works
Silva-Gomes, R., Mapelli, S. N., Boutet, M., Mattiola, I., Sironi, M., Grizzi, F., Colombo, F., Supino, D., Carnevale, S., Pasqualini, F., et al. (2021) · Journal of Leukocyte Biology · doi:10.1002/jlb.2a0421-200r · Cited by 55 · see citing works
Kamio, M., Yambe, H., & Fusetani, N. (2021) · Fisheries Science · doi:10.1007/s12562-021-01563-0 · Cited by 56 · see citing works
Common principles for odour coding across vertebrates and invertebrates
Fulton, K. A., Zimmerman, D., Samuel, A., Vogt, K., & Datta, S. R. (2024) · Nature reviews. Neuroscience · doi:10.1038/s41583-024-00822-0 · Cited by 51 · see citing works
Disruptive physiology: olfaction and the microbiome–gut–brain axis
Bienenstock, J., Kunze, W., & Forsythe, P. (2017) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12348 · Cited by 52 · see citing works
Neural circuits regulating sexual behaviors via the olfactory system in mice
Ishii, K. K., & Touhara, K. (2018) · Neuroscience Research · doi:10.1016/j.neures.2018.10.009 · Cited by 53 · see citing works
Vilela, A., Bacelar, E. L. V. A., Pinto, T., Anjos, R., Correia, E., Gonçalves, B. C., & Cosme, F. (2019) · Foods · doi:10.3390/foods8120643 · Cited by 50 · see citing works
Olfaction across the water–air interface in anuran amphibians
Weiß, L., Manzini, I., & Hassenklöver, T. (2021) · Cell and Tissue Research · doi:10.1007/s00441-020-03377-5 · Cited by 47 · see citing works
Pluskal, T., & Weng, J. (2017) · Chemical Society Reviews · doi:10.1039/c7cs00411g · Cited by 46 · see citing works
Genetic risk factors for Alzheimer disease: emerging roles of microglia in disease pathomechanisms
Takatori, S., Wang, W., Iguchi, A., & Tomita, T. (2019) · Advances in Experimental Medicine and Biology · doi:10.1007/978-3-030-05542-4_5 · Cited by 44 · see citing works
Excreted Steroids in Vertebrate Social Communication
Doyle, W. I., & Meeks, J. P. (2018) · Journal of Neuroscience · doi:10.1523/jneurosci.2488-17.2018 · Cited by 45 · see citing works
Novel Targets for Alzheimer's Disease: A View Beyond Amyloid
Ray, W. J., & Buggia-Prévot, V. (2020) · Annual Review of Medicine · doi:10.1146/annurev-med-052919-120219 · Cited by 43 · see citing works
Ma, S., Bi, W., Liu, X., Li, S., Qiu, Y., Huang, C., Lv, R., & Yin, Q. (2022) · Frontiers in Endocrinology · doi:10.3389/fendo.2022.891039 · Cited by 43 · see citing works
Functional evolution of vertebrate sensory receptors
Baldwin, M. W., & Ko, M. (2020) · Hormones and Behavior · doi:10.1016/j.yhbeh.2020.104771 · Cited by 43 · see citing works
Non-Canonical Odor Coding in the MosquitoPreprint
Younger, M. A., Herre, M., Goldman, O. V., Lu, T., Caballero-Vidal, G., Qi, Y., Gilbert, Z. N., Gong, Z., Morita, T., Rahiel, S., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.11.07.368720 · Cited by 43 · see citing works
Qiu, Q., Wu, Y., Ma, L., Xu, W., Hills, M. H., Ramalingam, V., & Yu, C. R. (2021) · eLife · doi:10.7554/elife.60546 · Cited by 42 · see citing works
Olfactory signaling via trace amine-associated receptors
Dewan, A. (2020) · Cell and Tissue Research · doi:10.1007/s00441-020-03331-5 · Cited by 41 · see citing works
A 3D transcriptomics atlas of the mouse nose sheds light on the anatomical logic of smell
Segura, M. L. R. T., Moussa, E. A., Garabello, E., Nakahara, T. S., Makhlouf, M., Mathew, L. S., Wang, L., Valle, F., Huang, S. S. Y., Mainland, J. D., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110547 · Cited by 37 · see citing works
The role of metals in mammalian olfaction of low molecular weight organosulfur compounds
Block, E., Batista, V. S., Matsunami, H., Zhuang, H., & Ahmed, L. (2017) · Natural Product Reports · doi:10.1039/c7np00016b · Cited by 37 · see citing works
Sex differences in main olfactory system pathways involved in psychosexual function
Cherry, J. A., & Baum, M. J. (2019) · Genes Brain & Behavior · doi:10.1111/gbb.12618 · Cited by 34 · see citing works
Yang, L. M., Huh, S., & Ornitz, D. M. (2018) · Developmental Cell · doi:10.1016/j.devcel.2018.07.010 · Cited by 33 · see citing works
Polymodal sensory perception drives settlement and metamorphosis of Ciona larvae
Høyer, J., Kolar, K., Athira, A., van den Burgh, M., Dondorp, D. C., Liang, Z., & Chatzigeorgiou, M. (2024) · Current Biology · doi:10.1016/j.cub.2024.01.041 · Cited by 31 · see citing works
Coordination of two enhancers drives expression of olfactory trace amine-associated receptors
Fei, A., Wu, W., Tan, L., Tang, C., Xu, Z., Huo, X., Bao, H., Kong, Y., Johnson, M. A., Hartmann, G. G., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-23823-4 · Cited by 30 · see citing works
Identifying Isl1 Genetic Lineage in the Developing Olfactory System and in GnRH-1 Neurons
Taroc, E. Z. M., Katreddi, R. R., & Forni, P. E. (2020) · Frontiers in Physiology · doi:10.3389/fphys.2020.601923 · Cited by 23 · see citing works
Koike, K., Yoo, S., Bleymehl, K., Omura, M., Zapiec, B., Pyrski, M. M., Blum, T. S., Khan, M., Bai, Z., Leinders‐Zufall, T., et al. (2021) · Neuron · doi:10.1016/j.neuron.2021.05.032 · Cited by 27 · see citing works
Paoli, M., Münch, D., Haase, A., Skoulakis, E., Turin, L., & Galizia, C. G. (2017) · eneuro · doi:10.1523/eneuro.0070-17.2017 · Cited by 27 · see citing works
Social modulation of fear: Facilitation vs buffering
Morozov, A., & Ito, W. (2018) · Genes Brain & Behavior · doi:10.1111/gbb.12491 · Cited by 27 · see citing works
Lacher, S. E., Alazizi, A., Wang, X., Bell, D. A., Piqué-Regi, R., Luca, F., & Slattery, M. G. (2017) · Redox Biology · doi:10.1016/j.redox.2017.10.018 · Cited by 26 · see citing works
Hirata, T., Shioi, G., Abe, T., Kiyonari, H., Kato, S., Kobayashi, K., Mori, K., & Kawasaki, T. (2019) · eNeuro · doi:10.1523/eneuro.0234-19.2019 · Cited by 27 · see citing works
Korsching, S. I. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.24155-2 · Cited by 25 · see citing works
Guo, L., Dai, W., Xu, Z., Liang, Q., Miller, E. T., Li, S., Gao, X., Baldwin, M. W., Chai, R., & Li, Q. (2022) · Molecular Biology and Evolution · doi:10.1093/molbev/msac006 · Cited by 25 · see citing works
Odorant organization in the olfactory bulb of the sea lamprey
Green, W. W., Boyes, K. C., McFadden, C., Daghfous, G., Auclair, F., Zhang, H., Li, W., Dubuc, R., & Zielinski, B. S. (2017) · Journal of Experimental Biology · doi:10.1242/jeb.150466 · Cited by 23 · see citing works
Calcium-activated chloride channels clamp odor-evoked spike activity in olfactory receptor neurons
Zak, J. D., Grimaud, J., Li, R.-C., Lin, C.-C., & Murthy, V. N. (2018) · Scientific Reports · doi:10.1038/s41598-018-28855-3 · Cited by 24 · see citing works
Brush cells, the newly identified gatekeepers of the urinary tract
Kummer, W., & Deckmann, K. (2016) · Current Opinion in Urology · doi:10.1097/mou.0000000000000361 · Cited by 23 · see citing works
The Role of Olfactory Genes in the Expression of Rodent Paternal Care Behavior
Rymer, T. L. (2020) · Genes · doi:10.3390/genes11030292 · Cited by 22 · see citing works
The Grueneberg ganglion controls odor-driven food choices in mice under threat
Brechbühl, J., de Vallière, A., Wood, D., Nenniger-Tosato, M., & Broillet, M.-C. (2020) · Communications Biology · doi:10.1038/s42003-020-01257-w · Cited by 22 · see citing works
Sex steroid hormone synthesis, metabolism, and the effects on the mammalian olfactory system
Abaffy, T., Lu, H.-Y., & Matsunami, H. (2022) · Cell and Tissue Research · doi:10.1007/s00441-022-03707-9 · Cited by 21 · see citing works
Olfactory subsystems associated with the necklace glomeruli in rodents
Zimmerman, A. D., & Munger, S. D. (2021) · Cell and Tissue Research · doi:10.1007/s00441-020-03388-2 · Cited by 20 · see citing works
Regulatory Features for Odorant Receptor Genes in the Mouse Genome
Degl’Innocenti, A., & D’Errico, A. (2017) · Frontiers in Genetics · doi:10.3389/fgene.2017.00019 · Cited by 18 · see citing works
Arthur, G. K., Ehrhardt-Humbert, L. C., Snider, D. B., Jania, C. M., Tilley, S. L., Metcalfe, D. D., & Cruse, G. (2020) · Cellular Signalling · doi:10.1016/j.cellsig.2020.109617 · Cited by 18 · see citing works
Rosner, D., Sun, J., Cacace, R., Yee, A., Wagh, C., Rychkova, A., Dunlap, M., Gulbranson, D. R., Ibrahim, A., Wang, X., et al. (2025) · Neuron · doi:10.1016/j.neuron.2025.11.022 · Cited by 20 · see citing works
Kyani-Rogers, T., Philbrook, A., McLachlan, I. G., Flavell, S. W., O’Donnell, M. P., & Sengupta, P. (2022) · Genetics · doi:10.1093/genetics/iyac143 · Cited by 16 · see citing works
Olfaction and Pheromones: Uncanonical Sensory Influences and Bulbar Interactions
Vargas‐Barroso, V., Peña‐Ortega, F., & Larriva-Sahd, J. A. (2017) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2017.00108 · Cited by 14 · see citing works
Implications for human odor sensing revealed from the statistics of odorant-receptor interactions
Bak, J. H., Jang, S., & Hyeon, C. (2018) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1006175 · Cited by 14 · see citing works
Philbrook, A., O’Donnell, M. P., Grunenkovaite, L., & Sengupta, P. (2024) · PLoS Biology · doi:10.1371/journal.pbio.3002892 · Cited by 12 · see citing works
MS4A superfamily molecules in tumors, Alzheimer’s and autoimmune diseases
Luo, X., Luo, B., Fei, L., Zhang, Q., Liang, X., Chen, Y., & Zhou, X. (2024) · Frontiers in Immunology · doi:10.3389/fimmu.2024.1481494 · Cited by 13 · see citing works
Epigenetic programming of stochastic olfactory receptor choice
Yusuf, N., & Monahan, K. D. (2024) · genesis · doi:10.1002/dvg.23593 · Cited by 12 · see citing works
Olfactory subsystems in the peripheral olfactory organ of anuran amphibians
Jungblut, L. D., Reiss, J. O., & Pozzi, A. G. (2020) · Cell and Tissue Research · doi:10.1007/s00441-020-03330-6 · Cited by 12 · see citing works
A purely bioinformatic pipeline for the prediction of mammalian odorant receptor gene enhancers
Degl’Innocenti, A., Meloni, G., Mazzolai, B., & Ciofani, G. (2019) · BMC Bioinformatics · doi:10.1186/s12859-019-3012-1 · Cited by 11 · see citing works
From odor to oncology: non-canonical odorant receptors in cancer
Park, S. J., Greer, P. L., & Lee, N. (2023) · Oncogene · doi:10.1038/s41388-023-02908-y · Cited by 11 · see citing works
Inhibitory actions of melanin‐concentrating hormone in the lateral septum
Payant, M. A., Spencer, C. D., Ly, N. K. K., & Chee, M. J. S. (2024) · The Journal of Physiology · doi:10.1113/jp284845 · Cited by 10 · see citing works
Severi, I., Perugini, J., Ruocco, C., Coppi, L., Pedretti, S., Mercurio, E. D., Senzacqua, M., Ragni, M., Imperato, G., Valerio, A., et al. (2023) · Molecular Metabolism · doi:10.1016/j.molmet.2023.101862 · Cited by 12 · see citing works
Bashkirova, E., Monahan, K., Campbell, C. E., Osinski, J. M., Tan, L., Schieren, I., Barnea, G., Xie, X. S., Gronostajski, R. M., & Lomvardas, S. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.08.30.274035 · Cited by 10 · see citing works
Odor Coding in the Mammalian Olfactory EpitheliumPreprint
Kurian, S. M., Naressi, R. G., Manoel, D., Barwich, A., Malnic, B., & Saraiva, L. R. (2020) · doi:10.31234/osf.io/pdnwy · Cited by 10 · see citing works
Jiang, H.-C., Park, S. J., Wang, I., Bear, D. M., Nowlan, A. C., & Greer, P. L. (2024) · Nature Communications · doi:10.1038/s41467-024-47698-3 · Cited by 8 · see citing works
Prospects on non-canonical olfaction in the mosquito and other organisms: why co-express?
Fernández-Chiappe, F., Ocker, G. K., & Younger, M. A. (2024) · Current Opinion in Insect Science · doi:10.1016/j.cois.2024.101291 · Cited by 8 · see citing works
In situ hybridization analysis of olfactory receptor expression in the sea turtle olfactory organ
Nakamuta, S., Mori, M., Ito, M., Kurita, M., Miyazaki, M., Yamamoto, Y., & Nakamuta, N. (2023) · Cell and Tissue Research · doi:10.1007/s00441-023-03782-6 · Cited by 8 · see citing works
Multimodal learning of pheromone locations
Pardasani, M., Marathe, S. D., Purnapatre, M., Dalvi, U., & Abraham, N. M. (2019) · bioRxiv · doi:10.1096/fj.202100167r · Cited by 10 · see citing works
de Vallière, A., Lopes, A. C., Addorisio, A., Gilliand, N., Nenniger-Tosato, M., Wood, D., Brechbühl, J., & Broillet, M.-C. (2022) · Frontiers in Nutrition · doi:10.3389/fnut.2022.1026373 · Cited by 8 · see citing works
Establishment and maintenance of random monoallelic expression
Kanata, E., Duffié, R., & Schulz, E. G. (2024) · Development · doi:10.1242/dev.201741 · Cited by 7 · see citing works
Chen, Y., Li, S., Huang, X., Wang, C., Pan, Y., Xiang, Q., Feng, Z., Fei, L., Wu, Y., Ruan, Z., et al. (2023) · Molecular Immunology · doi:10.1016/j.molimm.2023.07.003 · Cited by 7 · see citing works
Shahriari, A., Aoudi, B., & Tierney, K. B. (2023) · Aquaculture and Fisheries · doi:10.1016/j.aaf.2023.05.011 · Cited by 7 · see citing works
Renewal and Differentiation of GCD Necklace Olfactory Sensory Neurons
Bloom, M. L., Johnston, L. B., & Datta, S. R. (2020) · Chemical Senses · doi:10.1093/chemse/bjaa027 · Cited by 7 · see citing works
Conservation of Glomerular Organization in the Main Olfactory Bulb of Anuran Larvae
Weiß, L., Jungblut, L. D., Pozzi, A. G., O’Connell, L. A., Hassenklöver, T., & Manzini, I. (2020) · Frontiers in Neuroanatomy · doi:10.3389/fnana.2020.00044 · Cited by 7 · see citing works
Dalton, R. P. (2018) · F1000Research · doi:10.12688/f1000research.13659.1 · Cited by 6 · see citing works
Subcellular localization of MS4A13 isoform 2 in mouse spermatozoa
Kaneko, T., Toshimori, K., & Iida, H. (2017) · Reproduction · doi:10.1530/rep-17-0477 · Cited by 6 · see citing works
The Functional Characterization of GCaMP3.0 Variants Specifically Targeted to Subcellular Domains
Kempmann, A., Gensch, T., Offenhäusser, A., Tihaa, I., Maybeck, V., Balfanz, S., & Baumann, A. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms23126593 · Cited by 6 · see citing works
Evolution of Neurosensory Cells and Systems
Fritzsch, B., & Elliott, K. L. (2022) · CRC Press eBooks · doi:10.1201/9781003092810 · Cited by 5 · see citing works
Odor representation and coding by the mitral/tufted cells in the olfactory bulb
Wang, P., Li, S., & Li, A. (2024) · Journal of Zhejiang University SCIENCE B · doi:10.1631/jzus.b2400051 · Cited by 5 · see citing works
Genome-scale investigation of olfactory system spatial heterogeneity
Noto, T., Barnagian, D., & Castro, J. B. (2017) · PLoS ONE · doi:10.1371/journal.pone.0178087 · Cited by 5 · see citing works
Evolution of Pheromones in Mammals
Voznessenskaya, V. V., Klyuchnikova, M. A., & Laktionova, T. K. (2022) · Biology Bulletin Reviews · doi:10.1134/s2079086422010091 · Cited by 5 · see citing works
Lutz, M. W., & Chiba‐Falek, O. (2023) · Alzheimer s & Dementia · doi:10.1002/alz.13168 · Cited by 4 · see citing works
Makhlouf, M., D’Hulst, C., Omura, M., Rosa, A., Mina, R., Bernal-Garcia, S., Lempert, E., Saraiva, L. R., & Feinstein, P. G. (2025) · Cell Reports · doi:10.1016/j.celrep.2025.115955 · Cited by 4 · see citing works
Compartmentalization of the Mammalian Olfactory System
Fleischer, J., Strotmann, J. M., & Breer, H. (2020) · Elsevier eBooks · doi:10.1016/b978-0-12-809324-5.23877-7 · Cited by 4 · see citing works
Serafin, E. K., Burns, R., Yoo, J. J., & Baccei, M. L. (2021) · PAIN Reports · doi:10.1097/pr9.0000000000000947 · Cited by 4 · see citing works
A Testis ER Chaperone Marks Mature Olfactory and Vomeronasal Sensory NeuronsPreprint
Dalton, R. P. (2017) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/237719 · Cited by 4 · see citing works
When noncanonical olfaction is optimal
Lienkaemper, C., Younger, M. A., & Ocker, G. K. (2025) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2508439122 · Cited by 3 · see citing works
Airway sensory systems: breathing new life into microbiota-brain communication
Mann‐Nüttel, R., Armbruster, M., Mandal, S., & Forsythe, P. (2025) · Frontiers in Cellular Neuroscience · doi:10.3389/fncel.2025.1632805 · Cited by 4 · see citing works
- Authors
- Greer, P. L., Bear, D. M., Lassance, J.-M., Bloom, M. L., Tsukahara, T., Pashkovski, S. L., Masuda, F. K., Nowlan, A. C., Kirchner, R., Hoekstra, H. E., & Datta, S. R.
- Affiliations
- Harvard University (US)
- Howard Hughes Medical Institute (US)
- Corresponding author
- Datta, Sandeep Robert
- ORCID
- Venue
- Cell
- Publisher
- Elsevier BV
- Published
- 2016-06
- Volume
- 165
- Issue
- 7
- Pages
- 1734-1748
- ISSN
- 0092-8674 (ISSN-L)
- PMC
- PMC4912422
- OpenAlex
- W2406818379
- Cited by
- 148
- References
- 70
- Citations by year
- 2026: 4 · 2025: 15 · 2024: 13 · 2023: 10 · 2022: 18 · 2021: 17 · 2020: 25 · 2019: 13 · 2018: 14 · 2017: 16 · 2016: 3
- FWCI
- 11.36
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Cell (publishedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- ORBi (University of Liège) (submittedVersion, cc-by)
- Funders
- National Science Foundation
- Alfred P. Sloan Foundation
- Belgian American Educational Foundation
- McKnight Foundation (DP2OD007109, RO11DC011558)
- Vallee Foundation
- Astellas Pharma
- Astellas Foundation for Research on Metabolic Disorders
- National Institutes of Health (1dp2od007109-01)
- Japan Society for the Promotion of Science
- National Institute on Drug Abuse (F31DA036922)
- National Institute on Deafness and Other Communication Disorders (R01DC011558)
- Topics
- Life Sciences › Neuroscience › Sensory Systems › Olfactory and Sensory Function Studies
- Life Sciences › Neuroscience › Sensory Systems › Ion Channels and Receptors
- Health Sciences › Nursing › Nutrition and Dietetics › Biochemical Analysis and Sensing Techniques
- Keywords
- olfactory sensory neurons, mammalian olfaction, pheromone detection, fatty acid detection, olfaction
- MeSH terms
- Animals, Membrane Proteins, Nerve Tissue Proteins, Odorants, Phylogeny, Smell, Olfactory Receptor Neurons, Mice
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
