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Shebanits, K., Günther, T., Johansson, A. C. V., Maqbool, K., Feuk, L., Jakobsson, M. & Larhammar, D. (2019). Copy number determination of the gene for the human pancreatic polypeptide receptor NPY4R using read depth analysis and droplet digital PCR.. BMC Biotechnology, 19, Article ID 31.
Open this publication in new window or tab >>Copy number determination of the gene for the human pancreatic polypeptide receptor NPY4R using read depth analysis and droplet digital PCR.
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2019 (English)In: BMC Biotechnology, ISSN 1472-6750, E-ISSN 1472-6750, Vol. 19, article id 31Article in journal (Refereed) Published
Abstract [en]

Background: Copy number variation (CNV) plays an important role in human genetic diversity and has been associated with multiple complex disorders. Here we investigate a CNV on chromosome 10q11.22 that spans NPY4R, the gene for the appetite-regulating pancreatic polypeptide receptor Y4. This genomic region has been challenging to map due to multiple repeated elements and its precise organization has not yet been resolved. Previous studies using microarrays were interpreted to show that the most common copy number was 2 per genome.

Results: We have investigated 18 individuals from the 1000 Genomes project using the well-established method of read depth analysis and the new droplet digital PCR (ddPCR) method. We find that the most common copy number for NPY4R is 4. The estimated number of copies ranged from three to seven based on read depth analyses with Control-FREEC and CNVnator, and from four to seven based on ddPCR. We suggest that the difference between our results and those published previously can be explained by methodological differences such as reference gene choice, data normalization and method reliability. Three high-quality archaic human genomes (two Neanderthal and one Denisova) display four copies of the NPY4R gene indicating that a duplication occurred prior to the human-Neanderthal/Denisova split.

Conclusions: We conclude that ddPCR is a sensitive and reliable method for CNV determination, that it can be used for read depth calibration in CNV studies based on already available whole-genome sequencing data, and that further investigation of NPY4R copy number variation and its consequences are necessary due to the role of Y4 receptor in food intake regulation.

National Category
Cell Biology Genetics
Identifiers
urn:nbn:se:uu:diva-356569 (URN)10.1186/s12896-019-0523-9 (DOI)000470281900001 ()31164119 (PubMedID)
Funder
Swedish Research CouncilThe Swedish Brain Foundation
Available from: 2018-08-01 Created: 2018-08-01 Last updated: 2019-06-25Bibliographically approved
Pedersen, J. E., Bergqvist, C. & Larhammar, D. (2019). Evolution of vertebrate nicotinic acetylcholine receptors. BMC Evolutionary Biology, 19, Article ID 38.
Open this publication in new window or tab >>Evolution of vertebrate nicotinic acetylcholine receptors
2019 (English)In: BMC Evolutionary Biology, ISSN 1471-2148, E-ISSN 1471-2148, Vol. 19, article id 38Article in journal (Refereed) Published
Abstract [en]

Background

Many physiological processes are influenced by nicotinic acetylcholine receptors (nAChR), ranging from neuromuscular and parasympathetic signaling to modulation of the reward system and long-term memory. Due to the complexity of the nAChR family and variable evolutionary rates among its members, their evolution in vertebrates has been difficult to resolve. In order to understand how and when the nAChR genes arose, we have used a broad approach of analyses combining sequence-based phylogeny, chromosomal synteny and intron positions.

Results

Our analyses suggest that there were ten subunit genes present in the vertebrate predecessor. The two basal vertebrate tetraploidizations (1R and 2R) then expanded this set to 19 genes. Three of these have been lost in mammals, resulting in 16 members today. None of the ten ancestral genes have kept all four copies after 2R. Following 2R, two of the ancestral genes became triplicates, five of them became pairs, and three seem to have remained single genes. One triplet consists of CHRNA7, CHRNA8 and the previously undescribed CHRNA11, of which the two latter have been lost in mammals but are still present in lizards and ray-finned fishes. The other triplet consists of CHRNB2, CHRNB4 and CHRNB5, the latter of which has also been lost in mammals. In ray-finned fish the neuromuscular subunit gene CHRNB1 underwent a local gene duplication generating CHRNB1.2. The third tetraploidization in the predecessor of teleosts (3R) expanded the repertoire to a total of 31 genes, of which 27 remain in zebrafish. These evolutionary relationships are supported by the exon-intron organization of the genes.

Conclusion

The tetraploidizations explain all gene duplication events in vertebrates except two. This indicates that the genome doublings have had a substantial impact on the complexity of this gene family leading to a very large number of members that have existed for hundreds of millions of years.

National Category
Evolutionary Biology Cell Biology Biochemistry and Molecular Biology Bioinformatics and Systems Biology
Identifiers
urn:nbn:se:uu:diva-353919 (URN)10.1186/s12862-018-1341-8 (DOI)000457255700002 ()30700248 (PubMedID)
Funder
The Swedish Brain FoundationCarl Tryggers foundation
Available from: 2018-06-18 Created: 2018-06-18 Last updated: 2019-02-25Bibliographically approved
Shebanits, K., Vasile, S., Xu, B., Gutiérrez-de-Terán, H. & Larhammar, D. (2019). Functional characterization in vitro of twelve naturally occurring variants of the human pancreatic polypeptide receptor NPY4R. Neuropeptides, Article ID 101933.
Open this publication in new window or tab >>Functional characterization in vitro of twelve naturally occurring variants of the human pancreatic polypeptide receptor NPY4R
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2019 (English)In: Neuropeptides, ISSN 0143-4179, E-ISSN 1532-2785, article id 101933Article in journal (Refereed) Published
Abstract [en]

Obesity has become a global health problem and therefore understanding of the mechanisms regulating hunger and satiety is of utmost importance for the development of new treatment strategies. The Y4 receptor, encoded by the NPY4R gene, and its ligand pancreatic polypeptide (PP) have been reported to mediate a satiety signal. Multiple genetic studies have reported an association between NPY4R copy number and body weight. The gene also displays several SNP variants, many of which lead to amino acid differences, making it interesting to study. We have investigated the functional properties of 12 naturally occurring amino acid sequence variants of the Y4 and interpret the results in relation to sequence conservation and our structural model of the human Y4 receptor protein. Three receptor variants, Cys201(ECL2)Tyr, Val271(6.41)Leu and Asn318(7.49)Asp, were found to completely lose functional response, measured as inositol phosphate turnover, while retaining membrane expression. They display high sequence conservation and have important roles in the receptor structure. For two receptor variants the potency of PP was significantly decreased, Cys34(NT)Ser (EC50 = 2.9 nM, p < .001) and Val135(3.46)Met (EC50 = 3.0 nM, p < .01), compared to wild-type Y4 (EC50 = 0.68 nM). Cys34 forms a disulphide bond with Cys298, linking the N-terminal part to ECL3. The Val135(3.46)Met variant has an amino acid replacement located in the TM3 helix, one helix turn above the highly conserved ERH motif. This position has influence on the network of residues involved in receptor activation and subsequent inactivation. Sequence conservation and the structural model are consistent with these results. The remaining seven positions had no significant effect on the receptor's functional response compared to wild-type Y4. These positions display more variation during evolution. Understanding of the interactions between the Y4 receptor and its native PP agonist and the effects of amino acid variation on its functional response will hopefully lead to future therapeutic possibilities.

Place, publisher, year, edition, pages
CHURCHILL LIVINGSTONE, 2019
Keywords
Y4, SNP, Mutagenesis, Functional pharmacology, Structural modelling
National Category
Biochemistry and Molecular Biology
Identifiers
urn:nbn:se:uu:diva-356572 (URN)10.1016/j.npep.2019.05.004 (DOI)31230758 (PubMedID)
Funder
Swedish Research Council, K2013-55 x -22189-01-2
Available from: 2018-08-01 Created: 2018-08-01 Last updated: 2019-10-23Bibliographically approved
Shebanits, K., Andersson-Assarsson, J. C., Larsson, I., Carlsson, L. M. S., Feuk, L. & Larhammar, D. (2018). Copy number of pancreatic polypeptide receptor gene NPY4R correlates with body mass index and waist circumference. PLoS ONE, 13(4), Article ID e0194668.
Open this publication in new window or tab >>Copy number of pancreatic polypeptide receptor gene NPY4R correlates with body mass index and waist circumference
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2018 (English)In: PLoS ONE, ISSN 1932-6203, E-ISSN 1932-6203, Vol. 13, no 4, article id e0194668Article in journal (Refereed) Published
Abstract [en]

Multiple genetic studies have linked copy number variation (CNV) in different genes to body mass index (BMI) and obesity. A CNV on chromosome 10q11.22 has been associated with body weight. This CNV region spans NPY4R, the gene encoding the pancreatic polypeptide receptor Y4, which has been described as a satiety-stimulating receptor. We have investigated CNV of the NPY4R gene and analysed its relationship to BMI, waist circumference and self-reported dietary intake from 558 individuals (216 men and 342 women) representing a wide BMI range. The copy number for NPY4R ranged from 2 to 8 copies (average 4.6 +/- 0.8). Rather than the expected negative correlation, we observed a positive correlation between NPY4R copy number and BMI as well as waist circumference (r = 0.267, p = 2.65x 10(-7) and r = 0.256, p = 8x10(-7), respectively). Each additional copy of NPY4R correlated with 2.6 kg/m(2) increase in BMI and 5.67 cm increase in waist circumference (p = 3.3x10(-7) and p = 1x10(-6), respectively) for women. For men, there was no statistically significant correlation between CNV and BMI. Our results suggest that NPY4R genetic variation influences body weight in women, but the exact role of this receptor appears to be more complex than previously proposed.

Place, publisher, year, edition, pages
PUBLIC LIBRARY SCIENCE, 2018
National Category
Genetics
Identifiers
urn:nbn:se:uu:diva-352692 (URN)10.1371/journal.pone.0194668 (DOI)000429206800023 ()29621259 (PubMedID)
Funder
Swedish Research Council, K2013-54X-11285-19Swedish Research Council, K2013-55X-22189-01-2The Swedish Brain Foundation, F02016-0217
Available from: 2018-06-08 Created: 2018-06-08 Last updated: 2019-01-03Bibliographically approved
Xu, B., Vasile, S., Østergaard, S., Paulsson, J. F., Pruner, J., Åqvist, J., . . . Larhammar, D. (2018). Elucidation of the Binding Mode of the Carboxyterminal Region of Peptide YY to the Human Y-2 Receptor. Molecular Pharmacology, 93(4), 323-334
Open this publication in new window or tab >>Elucidation of the Binding Mode of the Carboxyterminal Region of Peptide YY to the Human Y-2 Receptor
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2018 (English)In: Molecular Pharmacology, ISSN 0026-895X, E-ISSN 1521-0111, Vol. 93, no 4, p. 323-334Article in journal (Refereed) Published
Abstract [en]

Understanding the agonist-receptor interactions in the neuropeptide Y (NPY)/peptide YY (PYY) signaling system is fundamental for the design of novel modulators of appetite regulation. We report here the results of a multidisciplinary approach to elucidate the binding mode of the native peptide agonist PYY to the human Y2 receptor, based on computational modeling, peptide chemistry and in vitro pharmacological analyses. The preserved binding orientation proposed for full-length PYY and five analogs, truncated at the amino terminus, explains our pharmacological results where truncations of the N-terminal proline helix showed little effect on peptide affinity. This was followed by receptor mutagenesis to investigate the roles of several receptor positions suggested by the modeling. As a complement, PYY-(3-36) analogs were synthesized with modifications at different positions in the common PYY/NPY C-terminal fragment (32TRQRY36-amide). The results were assessed and interpreted by molecular dynamics and Free Energy Perturbation (FEP) simulations of selected mutants, providing a detailed map of the interactions of the PYY/NPY C-terminal fragment with the transmembrane cavity of the Y2 receptor. The amidated C-terminus would be stabilized by polar interactions with Gln2886.55 and Tyr2195.39, while Gln1303.32 contributes to interactions with Q34 in the peptide and T32 is close to the tip of TM7 in the receptor. This leaves the core, α-helix of the peptide exposed to make potential interactions with the extracellular loops. This model agrees with most experimental data available for the Y2 system and can be used as a basis for optimization of Y2 receptor agonists.

National Category
Biochemistry and Molecular Biology Pharmacology and Toxicology
Identifiers
urn:nbn:se:uu:diva-381397 (URN)10.1124/mol.117.110627 (DOI)000461898900005 ()29367257 (PubMedID)
Funder
Swedish Research Council, 521-2014-2118Novo NordiskeSSENCE - An eScience Collaboration
Available from: 2019-04-17 Created: 2019-04-17 Last updated: 2019-10-23Bibliographically approved
Elphick, M. R., Mirabeau, O. & Larhammar, D. (2018). Evolution of neuropeptide signalling systems. Journal of Experimental Biology, 221(3), Article ID jeb151092.
Open this publication in new window or tab >>Evolution of neuropeptide signalling systems
2018 (English)In: Journal of Experimental Biology, ISSN 0022-0949, E-ISSN 1477-9145, Vol. 221, no 3, article id jeb151092Article, review/survey (Refereed) Published
Abstract [en]

Neuropeptides are a diverse class of neuronal signalling molecules that regulate physiological processes and behaviour in animals. However, determining the relationships and evolutionary origins of the heterogeneous assemblage of neuropeptides identified in a range of phyla has presented a huge challenge for comparative physiologists. Here, we review revolutionary insights into the evolution of neuropeptide signalling that have been obtained recently through comparative analysis of genome/transcriptome sequence data and by 'deorphanisation' of neuropeptide receptors. The evolutionary origins of at least 30 neuropeptide signalling systems have been traced to the common ancestor of protostomes and deuterostomes. Furthermore, two rounds of genome duplication gave rise to an expanded repertoire of neuropeptide signalling systems in the vertebrate lineage, enabling neofunctionalisation and/or subfunctionalisation, but with lineage-specific gene loss and/or additional gene or genome duplications generating complex patterns in the phylogenetic distribution of paralogous neuropeptide signalling systems. We are entering a new era in neuropeptide research where it has become feasible to compare the physiological roles of orthologous and paralogous neuropeptides in a wide range of phyla. Moreover, the ambitious mission to reconstruct the evolution of neuropeptide function in the animal kingdom now represents a tangible challenge for the future.

Place, publisher, year, edition, pages
COMPANY OF BIOLOGISTS LTD, 2018
Keywords
Evolution, Invertebrate, Neuropeptide, Phylogeny, Receptor, Vertebrate
National Category
Evolutionary Biology
Identifiers
urn:nbn:se:uu:diva-348318 (URN)10.1242/jeb.151092 (DOI)000425021700009 ()
Funder
Swedish Research CouncilCarl Tryggers foundation
Available from: 2018-04-24 Created: 2018-04-24 Last updated: 2019-01-03Bibliographically approved
Ocampo Daza, D. & Larhammar, D. (2018). Evolution of the growth hormone, prolactin, prolactin 2 and somatolactin family. General and Comparative Endocrinology, 264, 94-112
Open this publication in new window or tab >>Evolution of the growth hormone, prolactin, prolactin 2 and somatolactin family
2018 (English)In: General and Comparative Endocrinology, ISSN 0016-6480, E-ISSN 1095-6840, Vol. 264, p. 94-112Article in journal (Refereed) Published
Abstract [en]

Growth hormone (GH), prolactin (PRL), prolactin 2 (PRL2) and somatolactin (SL) belong to the same hormone family and have a wide repertoire of effects including development, osmoregulation, metabolism and stimulation of growth. Both the hormone and the receptor family have been proposed to have expanded by gene duplications in early vertebrate evolution. A key question is how hormone-receptor preferences have arisen among the duplicates. The first step to address this is to determine the time window for these duplications. Specifically, we aimed to see if duplications resulted from the two basal vertebrate tetraploidizations (1R and 2R). GH family genes from a broad range of vertebrate genomes were investigated using a combination of sequence-based phylogenetic analyses and comparisons of synteny. We conclude that the PRL and PRL2 genes arose from a common ancestor in 1R/2R, as shown by neighboring gene families. No other gene duplicates were preserved from these tetraploidization events. The ancestral genes that would give rise to GH and PRL/PRL2 arose from an earlier duplication; most likely a local gene duplication as they are syntenic in several species. Likewise, some evidence suggests that SL arose from a local duplication of an ancestral GH/SL gene in the same time window, explaining the lack of similarity in chromosomal neighbors to GH, PRL or PRL2. Thus, the basic triplet of ancestral GH, PRL/ PRL2 and SL genes appear to be unexpectedly ancient. Following 1R/2R, only SL was duplicated in the teleost-specific tetraploidization 3R, resulting in SLa and SLb. These time windows contrast with our recent report that the corresponding receptor genes GHR and PRLR arose through a local duplication in jawed vertebrates and that both receptor genes duplicated further in 3R, which reveals a surprising asynchrony in hormone and receptor gene duplications.

Place, publisher, year, edition, pages
ACADEMIC PRESS INC ELSEVIER SCIENCE, 2018
Keywords
Growth hormone, Somatolactin, Prolactin, Prolactin 2, Gene duplication, Molecular evolution, Phylogeny
National Category
Physiology Zoology
Identifiers
urn:nbn:se:uu:diva-358261 (URN)10.1016/j.ygcen.2018.01.007 (DOI)000435889100011 ()29339183 (PubMedID)
Funder
Swedish Research CouncilCarl Tryggers foundation
Available from: 2018-08-27 Created: 2018-08-27 Last updated: 2019-01-03Bibliographically approved
Pedersen, J. E., Bergqvist, C. & Larhammar, D. (2018). Evolution of the muscarinic acetylcholine receptors in vertebrates. eNeuro, 5(5), Article ID UNSP e0340-18.2018.
Open this publication in new window or tab >>Evolution of the muscarinic acetylcholine receptors in vertebrates
2018 (English)In: eNeuro, ISSN 2373-2822, Vol. 5, no 5, article id UNSP e0340-18.2018Article in journal (Refereed) Published
Abstract [en]

The family of muscarinic acetylcholine receptors (mAChRs) consists of five members in mammals, encoded by theCHRM1-5 genes. The mAChRs are G-protein-coupled receptors, which can be divided into the following two subfamilies: M2 and M4 receptors coupling to Gi/o; and M1, M3, and M5 receptors coupling to Gq/11. However, despite the fundamental roles played by these receptors, their evolution in vertebrates has not yet been fully described. We have combined sequence-based phylogenetic analyses with comparisons of exon–intron organi- zation and conserved synteny in order to deduce the evolution of the mAChR receptors. Our analyses verify the existence of two ancestral genes prior to the two vertebrate tetraploidizations (1R and 2R). After these events, one gene had duplicated, resulting in CHRM2 and CHRM4; and the other had triplicated, forming the CHRM1,CHRM3, and CHRM5 subfamily. All five genes are still present in all vertebrate groups investigated except theCHRM1 gene, which has not been identified in some of the teleosts or in chicken or any other birds. Interestingly, the third tetraploidization (3R) that took place in the teleost predecessor resulted in duplicates of all five mAChR genes of which all 10 are present in zebrafish. One of the copies of the CHRM2 and CHRM3 genes and bothCHRM4 copies have gained introns in teleosts. Not a single separate (nontetraploidization) duplicate has been identified in any vertebrate species. These results clarify the evolution of the vertebrate mAChR family and reveal a doubled repertoire in zebrafish, inviting studies of gene neofunctionalization and subfunctionalization.

Keywords
acetylcholine, G-protein-coupled receptor, gene duplication, muscarinic, tetraploidization, zebrafish
National Category
Neurology
Research subject
Neuroscience
Identifiers
urn:nbn:se:uu:diva-371818 (URN)10.1523/ENEURO.0340-18.2018 (DOI)000456897300002 ()30564629 (PubMedID)
Funder
Carl Tryggers foundation
Note

De två första författarna delar förstaförfattarskapet.

Available from: 2019-01-02 Created: 2019-01-02 Last updated: 2019-02-18Bibliographically approved
Ocampo Daza, D. & Larhammar, D. (2018). Evolution of the receptors for growth hormone, prolactin, erythropoietin and thrombopoietin in relation to the vertebrate tetraploidizations. General and Comparative Endocrinology, 257, 143-160
Open this publication in new window or tab >>Evolution of the receptors for growth hormone, prolactin, erythropoietin and thrombopoietin in relation to the vertebrate tetraploidizations
2018 (English)In: General and Comparative Endocrinology, ISSN 0016-6480, E-ISSN 1095-6840, Vol. 257, p. 143-160Article in journal (Refereed) Published
Abstract [en]

The receptors for the pituitary hormones growth hormone (GH), prolactin (PRL) and somatolactin (SL), and the hematopoietic hormones erythropoietin (EPO) and thrombopoietin (TPO), comprise a structurally related family in the superfamily of cytokine class-I receptors. GH, PRL and SL receptors have a wide variety of effects in development, osmoregulation, metabolism and stimulation of growth, while EPO and TPO receptors guide the production and differentiation of erythrocytes and thrombocytes, respectively. The evolution of the receptors for GH, PRL and SL has been partially investigated by previous reports suggesting different time points for the hormone and receptor gene duplications. This raises questions about how hormone-receptor partnerships have emerged and evolved. Therefore, we have investigated in detail the expansion of this receptor family, especially in relation to the basal vertebrate (1R, 2R) and teleost (3R) tetraploidizations. Receptor family genes were identified in a broad range of vertebrate genomes and investigated using a combination of sequence-based phylogenetic analyses and comparative genomic analyses of synteny. We found that 1R most likely generated EPOR/TPOR and GHR/PRLR ancestors; following this, 2R resulted in EPOR and TPOR genes. No GHR/PRLR duplicate seems to have survived after 2R. Instead the single GHR/PRLR underwent a local duplication sometime after 2R, generating separate syntenic genes for GHR and PRLR. Subsequently, 3R duplicated the gene pair in teleosts, resulting in two GHR and two PRLR genes, but no EPOR or TPOR duplicates. These analyses help illuminate the evolution of the regulatory mechanisms for somatic growth, metabolism, osmoregulation and hematopoiesis in vertebrates.

Keywords
Growth hormone receptor, Prolactin receptor, Somatolactin receptor, Gene duplication, Molecular evolution, Phylogeny
National Category
Evolutionary Biology
Research subject
Biology with specialization in Molecular Evolution
Identifiers
urn:nbn:se:uu:diva-334515 (URN)10.1016/j.ygcen.2017.06.021 (DOI)000424858400016 ()28652136 (PubMedID)
Funder
Swedish Research CouncilCarl Tryggers foundation
Available from: 2017-11-23 Created: 2017-11-23 Last updated: 2018-04-18Bibliographically approved
Yang, Z., Han, S., Keller, M., Kaiser, A., Bender, B. J., Bosse, M., . . . Wu, B. (2018). Structural basis of ligand binding modes at the neuropeptide Y Y-1 receptor [Letter to the editor]. Nature, 556(7702), 520-524
Open this publication in new window or tab >>Structural basis of ligand binding modes at the neuropeptide Y Y-1 receptor
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2018 (English)In: Nature, ISSN 0028-0836, E-ISSN 1476-4687, Vol. 556, no 7702, p. 520-524Article in journal, Letter (Refereed) Published
Abstract [en]

Neuropeptide Y (NPY) receptors belong to the G-protein-coupled receptor superfamily and have important roles in food intake, anxiety and cancer biology(1,2). The NPY-Y receptor system has emerged as one of the most complex networks with three peptide ligands (NPY, peptide YY and pancreatic polypeptide) binding to four receptors in most mammals, namely the Y-1, Y-2, Y-4 and Y-5 receptors, with different affinity and selectivity(3). NPY is the most powerful stimulant of food intake and this effect is primarily mediated by the Y-1 receptor (Y1R)(4). A number of peptides and small-molecule compounds have been characterized as Y1R antagonists and have shown clinical potential in the treatment of obesity(4), tumour(1) and bone loss(5). However, their clinical usage has been hampered by low potency and selectivity, poor brain penetration ability or lack of oral bioavailability(6). Here we report crystal structures of the human Y1R bound to the two selective antagonists UR-MK299 and BMS-193885 at 2.7 and 3.0 angstrom resolution, respectively. The structures combined with mutagenesis studies reveal the binding modes of Y1R to several structurally diverse antagonists and the determinants of ligand selectivity. The Y1R structure and molecular docking of the endogenous agonist NPY, together with nuclear magnetic resonance, photo-crosslinking and functional studies, provide insights into the binding behaviour of the agonist and for the first time, to our knowledge, determine the interaction of its N terminus with the receptor. These insights into Y1R can enable structure-based drug discovery that targets NPY receptors.

National Category
Medicinal Chemistry
Identifiers
urn:nbn:se:uu:diva-354947 (URN)10.1038/s41586-018-0046-x (DOI)000430793000051 ()29670288 (PubMedID)
Funder
German Research Foundation (DFG), Be1264-16German Research Foundation (DFG), SFB 1052/A3German Research Foundation (DFG), KE 1857/1-1German Research Foundation (DFG), GRK 1910
Available from: 2018-06-25 Created: 2018-06-25 Last updated: 2019-01-03Bibliographically approved
Organisations
Identifiers
ORCID iD: ORCID iD iconorcid.org/0000-0002-6736-0663

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