{"database":"Pride","file_versions":[{"headers":{"Content-Type":["application/json"]},"body":{"files":{"Xlsx":["ftp://ftp.pride.ebi.ac.uk/pride/data/archive/2026/05/PXD062863/SampleTable.xlsx"],"Tabular":["ftp://ftp.pride.ebi.ac.uk/pride/data/archive/2026/05/PXD062863/SpectronautSearch.tsv"],"Txt":["ftp://ftp.pride.ebi.ac.uk/pride/data/archive/2026/05/PXD062863/SpectronautSearch.setup.txt","ftp://ftp.pride.ebi.ac.uk/pride/data/archive/2026/05/PXD062863/SpectronautSearch.log.txt"],"Fasta":["ftp://ftp.pride.ebi.ac.uk/pride/data/archive/2026/05/PXD062863/UniversalContaminantProteinFASTA.fasta","ftp://ftp.pride.ebi.ac.uk/pride/data/archive/2026/05/PXD062863/HomoSapien_Canonical_2024_10_26.fasta","ftp://ftp.pride.ebi.ac.uk/pride/data/archive/2026/05/PXD062863/contaminants.fasta"],"Other":["ftp://ftp.pride.ebi.ac.uk/pride/data/archive/2026/05/PXD062863/SpectronautSearch.params","ftp://ftp.pride.ebi.ac.uk/pride/data/archive/2026/05/PXD062863/MassSpectrometryFiles.zip"]},"type":"primary"},"statusCode":"OK","statusCodeValue":200}],"scores":null,"additional":{"labhead_mail":["ruthh@stanford.edu"],"submitter":["Dain Brademan"],"technology_type":["Mass Spectrometry","Bottom-up proteomics","Data-independent acquisition"],"software":[""],"submitter_keywords":["Mor","Opioids","Apex"],"full_dataset_link":["https://www.ebi.ac.uk/pride/archive/projects/PXD062863"],"tissue":["Hek-293t Cell"],"sample_protocol":["HEK293T cells expressing the APEX2 enzyme fused to the human MOR (MOR-APEX) and the spatial reference APEX constructs (for plasma membrane, early endosome, late endosome/lysosome, and cytoplasm as described previously1, were cultured in 6-well plate format and incubated with 500 μM biotin-phenol at 37 °C for 30 min. The receptor was activated with 10 μM DAMGO, 100 nM FNZ, and 100 nM DFNZ (all saturating concentrations) over a time course of 30 min. The spatial reference APEX samples were not treated with the ligands. APEX labeling was initiated pre-activation (time 0) and after 1, 5, 10 and 30 min of activation by 1:3 mixing of the H2O2 containing media (1 mM H2O2 final) with the biotin-phenol containing media at room temperature. After 45 s of the biotinylation reaction, the cells were washed three times (1 min each) with ice cold quench buffer (PBS supplemented with 10 mM sodium ascorbate, 10 mM sodium azide, and 5 mM Trolox). Cells were then collected in 1 mL of quench buffer and pelleted by centrifugation at 4 °C for 10 min at 3000 x g. For cell lysis, cells were homogenized using probe sonication in RIPA buffer (50 mM Tris, 150 mM NaCl, 1% Triton X-100, 0.25% sodium deoxycholate, 0.25% SDS, pH 7.4) supplemented with 10 mM sodium ascorbate, 10 mM sodium azide, 5 mM Trolox, 1 mM DTT, and protease inhibitors (Roche Complete). To remove the cell debris, cell lysate was centrifuged at 10,000 x g for 10 min, and the supernatant was taken for streptavidin enrichment of biotinylated proteins. The enrichment of biotinylated proteins was automated with the KingFisher Flex (Thermo Fisher Scientific) as described previously. Briefly, supernatants were incubated at 4 °C for 18 hrs with 15 μl magnetic streptavidin beads (Pierce™ Streptavidin Magnetic Beads, Thermo Fisher Scientific) which were pre-washed twice with RIPA buffer. Following incubation, beads were washed three times with RIPA buffer, one time with 1 M KCl, one time with 0.1 M Na2CO3, one time with 2 M urea in 50 mM Tris-HCl (pH 8) buffer, and two times with 50 mM Tris-HCl (pH 8) buffer. Beads were maintained in 100 μL of 2 M urea in 50 mM Tris-HCl (pH 8) buffer for on-bead digestion of proteins. Samples were reduced with 5 mM TCEP (Tris(2-carboxyethyl)phosphine) at 37 °C for 30 min, followed by alkylation with 5 mM IAA (Iodoacetamide) at room temperature in the dark for another 30 min, which was quenched by addition of DTT (Dithiothreitol, 5 mM final). For tryptic digestion, 0.5 μg trypsin and 0.25 μg LysC was added to beads and incubated with shaking at 37 °C for 6 hrs. Supernatants were taken and saved for desalting using NEST C18 MicroSpin columns. MOR-APEX and spatial APEX reference samples were analyzed on an TimsTOF HT mass spectrometry system (Bruker) coupled to a Vanquish Neo ultra high-pressure liquid chromatography (Thermo Fisher Scientific) interfaced via a CaptiveSpray2 nanoelectrospray source (Bruker). Samples were reconstituted in 0.1% formic acid and loaded onto a 15 cm x 75 μm I.D. Aurora CSI column (IonOpticks). Mobile phase A consisted of 0.1% FA, and mobile phase B consisted of 0.1% FA/80% ACN. Peptides were separated at a flow rate of 500 nl/min using a nonlinear gradient increasing buffer B from 2% to 80% over 23 minutes, followed by a 7 minute wash at 95% B and column equilibration. The mass spectrometer acquired data in dia-PASEF mode using a 75 ms TIMS ramp, a 1/K0 range of 0.72-1.5, and an m/z range of 100 - 1700. One TIMS precursor MS frame was followed by 9 dia-PASEF MS2 frames. Fragmentation windows had a mass width of 30 Da with an m/z overlap of 1 Da and were collected over an m/z range of 250-1325 and a 1/K0 range of 0.68-1.40."],"repository":["Pride"],"quantification_method":[""],"modification":[""],"data_protocol":["The DIA data were analyzed with Spectronaut (Biognosys, version 19.7) using direct DIA analysis default parameters for the identification and quantification of proteins. Normalization in Spectronaut was turned off. Data were searched against the Uniprot Human database (downloaded October, 2024). Transition ion intensities from Spectronaut were summarized to protein intensities using the MSstats (version 4.10.1) function dataProcess with default settings only high quality were used (featureSubset = \"highQuality\"). All proteins with only one quantified peptide were left out of further analysis. Each protein’s trend over the time course after DAMGO, FNZ, and DFNZ treatment was scored by fitting the log2 intensities with a continuous cubic-polynomial curve over time using the R functions lm and poly. To better fit the rapid changes, especially between time 0 and 1 minute, the collected timepoints were encoded by their ranks (1, 2, 3, 4, and 5 for 0, 1, 5, 10, and 30 minutes). The model included an additive term for the batch–a protein’s background intensity was expected and allowed to vary between batches. The time-dependent model was compared with a null-model that contained only the batch term using the R function anova to compute an F statistic and p-value. The maximum mean change between time 0 and any single later time, after imputing any missing values using the fitted model, was used as the maximum log2 fold change for that protein. Proteins were considered significant interactors with the MOR-APEX construct using thresholds a maximum log2 fold change > log2 (1.5) over the time series and p-value ≤ 0.05 from the ANOVA test.  To define location specific proteins, proteins that varied between spatial references were scored using the MSstats function ‘groupComparison’ to compare between each non redundant pair of spatial references. The input to MSstats was the entire set of spatial references with the MOR-APEX2 data excluded. MSstats reports pairwise differences in means as log2FC, and a pairwise P value calculated from a t-test assuming equal variance across all spatial references. A subset of 650 location-specific proteins was selected that could reliably distinguish locations by requiring P value < 0.005 and log2FC > 1.0 and observed intensity in all three replicates of at least one spatial reference greater than the 50th percentile of all observed protein intensities. For each MOR-APEX2 sample (each ligand, timepoints, and replicate), coefficients were calculated to estimate the contribution of each spatial reference to the observed protein intensity as described previously.1 First, protein intensities were scaled linearly between 0 and 1 by setting the maximum observed intensity (across all spatial reference and MOR-APEX2 samples) for each protein to 1.0, and all other observations were set to the ratio of observed/maximum for that protein. Missing values were set to zero. A matrix representing protein intensities in the spatial references for all observed proteins (F) was constructed using mean (per spatial reference) scaled intensity. The location-specific subset matrix (S) was extracted from F by using only the rows of F that match the 650 location-specific proteins. S was then appended with three additional columns composed of randomly sampled values from S to minimize the occurrence of low but non zero location coefficients where they were expected to be zero. Location coefficients for each MOR-APEX2 sample were then calculated using the nonnegative least-squares procedure in the R package nnls using the location-specific matrix S and the vector of location-specific protein scaled intensities from each MOR-APEX2 sample as inputs. We repeated this randomization and nnls procedure 1000 times and used the median value for final spatial reference coefficients."],"omics_type":["Proteomics"],"labhead":["Ruth Huttenhain, PhD"],"instrument_platform":[""],"labhead_affiliation":["Department of Molecular & Cellular Physiology Stanford University School of Medicine"],"submission_type":["PARTIAL"],"species":["Homo Sapiens (human)"],"submitter_mail":["brademan@stanford.edu"],"publication":["41922775 Gomez JL, Ventriglia EN, Frangos ZJ, Sulima A, Robertson MJ, Sacco MD, Budinich RC, Giosan IM, Xie T, Solis O, Tischer AE, Bossert JM, Caldwell KE, Bonbrest H, Essmann A, Garçon-Poca ZM, Choi S, Noya MR, Limiac F, Arce A, Glatfelter GC, Robinson M, Chen L, Mullarkey AA, Brademan DR, Enten G, Dunne W, Quiroz C, Schoenborn I, Lee CB, Rais R, Holt DP, Dannals RF, Shi L, Hüttenhain R, Ferré S, Kiyatkin E, Bonaventura J, Shaham Y, Zachariou V, Baumann MH, Skiniotis G, Rice KC, Michaelides M. A µ-opioid receptor superagonist analgesic with minimal adverse effects. Nature. 2026 652(8112):1393-1404 10.1038/s41586-026-10299-9"],"submitter_affiliation":["Stanford School of Medicine\nMolecular and Cellular Physiology"],"submitter_country":["United States"],"pubmed_abstract":["Developing safe and effective pain medications is an ongoing challenge for human health. Agonists for the µ-opioid receptor (MOR) are essential pain medications, but their high intrinsic efficacy also induces adverse side effects, including respiratory depression, constipation, tolerance, dependence, withdrawal and addiction<sup>1-7</sup>. Strategies to limit adverse effects traditionally include developing MOR agonists that have low intrinsic efficacy or that preferentially activate G-protein signalling over β-arrestin signalling<sup>8</sup>. Here we identify a novel MOR agonist with supramaximal intrinsic efficacy and a unique pharmacological profile that produced effective analgesia in rodents with minimal adverse effects. N-desethyl-fluornitrazene (DFNZ) was derived from a class of synthetic benzimidazole opioids called nitazenes. DFNZ has impaired brain penetrance, a unique spatiotemporal MOR cellular signalling profile, and diminished efficacy at the MOR-galanin 1 receptor (GAL1) heteromer. DFNZ does not induce respiratory depression, tolerance or MOR downregulation after repeated exposure. Compared with other MOR agonists, DFNZ has limited effects on dopamine neurotransmission in nucleus accumbens and weaker reinforcing effects in the drug self-administration procedure. These results provide novel insights about MOR and nitazene pharmacology, have important implications for pain and addiction treatment, and challenge the prevailing dogma that high-efficacy MOR agonists cannot constitute safe and effective therapeutic agents."],"pubmed_title":["A µ-opioid receptor superagonist analgesic with minimal adverse effects."],"pubmed_authors":["Gomez Juan L JL, Ventriglia Emilya N EN, Frangos Zachary J ZJ, Sulima Agnieszka A, Robertson Michael J MJ, Sacco Michael D MD, Budinich Reece C RC, Giosan Ilinca M IM, Xie Tongzhen T, Solis Oscar O, Tischer Anna E AE, Bossert Jennifer M JM, Caldwell Kiera E KE, Bonbrest Hannah H, Essmann Amelie A, Garçon-Poca Zelai M ZM, Choi Shinbe S, Noya Michael R MR, Limiac Feonil F, Arce Ali A, Glatfelter Grant C GC, Robinson Margaret M, Chen Li L, Mullarkey Angelina A AA, Brademan Dain R DR, Enten Garrett G, Dunne William W, Quiroz César C, Schoenborn Ingrid I, Lee Chae Bin CB, Rais Rana R, Holt Daniel P DP, Dannals Robert F RF, Shi Lei L, Hüttenhain Ruth R, Ferré Sergi S, Kiyatkin Eugene E, Bonaventura Jordi J, Shaham Yavin Y, Zachariou Venetia V, Baumann Michael H MH, Skiniotis Georgios G, Rice Kenner C KC, Michaelides Michael M"],"additional_accession":[]},"is_claimable":false,"name":"A mu opioid receptor superagonist that produces analgesia with minimal adverse effects","description":"Developing safe and effective pain medications is an ongoing challenge for human health. Mu opioid receptor (MOR) agonists are essential pain medications, but their high intrinsic efficacy induces adverse side effects, including respiratory depression, constipation, tolerance, dependence, withdrawal, and addiction. Strategies to limit such effects traditionally include developing MOR agonists that have low intrinsic efficacy or preferentially activate G protein over β-arrestin signaling. We report the discovery of a novel MOR superagonist with supraphysiological intrinsic efficacy and a unique pharmacological profile that produces effective analgesia in rodents with minimal adverse side effects. N-desethyl-fluornitrazene (DFNZ) was derived from a class of synthetic benzimidazole opioids called Nitazenes. DFNZ has a unique spatiotemporal MOR cellular signaling profile that favors G protein activation over β-arrestin recruitment, impaired brain penetrance, and diminished efficacy at the MOR-galanin 1 receptor (Gal1R) heteromer. DFNZ does not induce respiratory depression, tolerance, or MOR desensitization after repeated exposure. Compared to other MOR agonists, DFNZ does not increase dopamine transmission in nucleus accumbens and has weaker reinforcing effects in the drug self-administration procedure. These results provide novel insights on MOR pharmacology, have important implications for pain and addiction treatment, and challenge the prevailing dogma that MOR superagonists cannot constitute safe and effective therapeutics.","dates":{"publication":"2026-05-25","submission":"2025-04-11"},"accession":"PXD062863","cross_references":{"TAXONOMY":["NEWT:330879","NEWT:377960","NEWT:1131","NEWT:35795","NEWT:2042546","NEWT:259447","NEWT:295546","NCBITaxon:2719036","NEWT:1334565","NEWT:625351","NEWT:258594","NCBITaxon:1280","NEWT:112503","NEWT:1129","NEWT:309807","NEWT:59753","NEWT:89184","NEWT:309800","NEWT:281395","NEWT:247480","NEWT:1211601","NEWT:876138","NEWT:44271","NEWT:193516","NEWT:2315688","NEWT:1073882","NEWT:6819","NEWT:475174","NEWT:1599","NEWT:428386","NEWT:1117","NEWT:498257","NEWT:10036","NEWT:32264","NEWT:12215","NEWT:1590","NEWT:10034","NEWT:33114","NEWT:1596","NEWT:661410","NEWT:638632","NEWT:224326","NEWT:376619","NCBITaxon:79857","NEWT:1096976","NEWT:3765","NEWT:3767","NEWT:1589","NEWT:135622","NEWT:4615","NEWT:672127","NEWT:35786","NEWT:1580","NEWT:399784","NEWT:96731","NEWT:656064","NEWT:1582","NEWT:3760","NEWT:1584","NEWT:36630","NEWT:1585","NEWT:383379","NEWT:381198","NEWT:418106","NCBITaxon:12721","NEWT:10029","NEWT:913645","NEWT:641809","NEWT:1392488","NEWT:38815","NEWT:317447","NEWT:4688","NEWT:7719","NEWT:5530","NEWT:868565","NEWT:135674","NEWT:79329","NEWT:30069","NEWT:12637","NEWT:59729","NEWT:2164133","NEWT:295105","NEWT:108061","NEWT:60711","NEWT:224308","NEWT:3347","NEWT:49928","NEWT:3349","NEWT:160621","NEWT:212790","NEWT:110368","NEWT:1310161","NEWT:77133","NEWT:145481","NEWT:1310165","NEWT:29058","NCBITaxon:79824","NEWT:410658","NEWT:5516","NEWT:44688","NEWT:44689","NEWT:498211","NEWT:345076","NEWT:347256","NEWT:5518","NEWT:398007","NEWT:1527468","NEWT:498217","NEWT:498216","NEWT:11320","NEWT:246196","NEWT:246197","NEWT:145458","NEWT:1310173","NEWT:200795","NEWT:2579791","NEWT:44685","NEWT:161934","NEWT:1148","NEWT:5508","NEWT:3329","NEWT:419481","NEWT:5507","NEWT:260499","NEWT:410661","NEWT:1140","NCBITaxon:2157","NEWT:2066563","NEWT:1143","NEWT:1287689","NEWT:1094343","NEWT:1462472","NEWT:1336795","NEWT:644042","NEWT:150808","NEWT:1182590","NEWT:3712","NEWT:3711","NEWT:3714","NCBITaxon:37162","NEWT:270643","NEWT:3715","NEWT:2065263","NEWT:177437","NEWT:717966","NEWT:10891","NEWT:10418","NEWT:118698","NEWT:1616117","NEWT:118696","NEWT:34865","NEWT:52283","NEWT:28174","NEWT:284812","NEWT:8175","NEWT:43330","NEWT:1603293","NEWT:44664","NEWT:43346","NEWT:3702","NEWT:1245466","NEWT:3704","NEWT:244366","NEWT:1246791","NEWT:176597","NEWT:118694","NEWT:2850","NEWT:118691","NEWT:34871","NEWT:9006","NEWT:33548","NEWT:52299","NEWT:8165","NEWT:96794","NEWT:3708","NEWT:332648","NEWT:44670","NEWT:926571","NEWT:536231","NEWT:376219","NEWT:219813","NEWT:1510","NEWT:460519","NEWT:1515","NEWT:572307","NEWT:1432138","NEWT:1424507","NEWT:1194599","NEWT:272844","NEWT:1348799","NEWT:33995","NEWT:55784","NEWT:1303443","NEWT:9483","NEWT:485","NEWT:56636","NEWT:2499525","NEWT:2853422","NEWT:487","NEWT:1538553","NEWT:1679718","NEWT:480","NEWT:67767","NEWT:45972","NEWT:46835","NEWT:109757","NEWT:582580","NEWT:1185650","NEWT:216778","NEWT:1502","NEWT:128017","NEWT:2836","NEWT:376686","NEWT:237610","NEWT:95486","EFO:0001352","NEWT:119562","NEWT:1883446","NEWT:1233435","NEWT:118223","NEWT:11757","NEWT:987059","NEWT:109760","NEWT:29031","NEWT:317047","NEWT:1509","NEWT:491","NEWT:460523","NEWT:45954","NEWT:235443","NEWT:1579","NEWT:1757312","NEWT:85694","NEWT:109786","NEWT:108458","NEWT:5936","NEWT:321967","NEWT:320637","NEWT:1078283","NEWT:3750","NEWT:983964","NEWT:11706","NEWT:32644","NEWT:527796","NEWT:499175","NEWT:109779","NEWT:3745","NEWT:1715989","NCBITaxon:4751","NEWT:3747","NEWT:1116234","NEWT:415978","NEWT:1255228","NEWT:410289","NEWT:191701","NEWT:373153","NEWT:1640278","NEWT:472","NEWT:940825","NEWT:29459","NEWT:529507","NEWT:1071661","NEWT:28128","NEWT:470","NEWT:41122","NEWT:5911","NEWT:748693","NCBITaxon:50557","NEWT:39251","NEWT:29491","NEWT:101841","NEWT:446","NEWT:153481","NEWT:2014887","NEWT:33952","NEWT:11723","NEWT:445","NEWT:153009","NEWT:261756","NEWT:166313","NEWT:63366","NEWT:63367","NEWT:29488","NEWT:215402","NEWT:1547","NEWT:1290454","NEWT:3726","NEWT:906914","NEWT:81231006","NEWT:28141","NEWT:9031","NEWT:27292","NEWT:1050722","NEWT:3728","NEWT:108931","NEWT:1293497","NEWT:1055524","NEWT:548","NEWT:150475","NEWT:267872","NEWT:381666","NEWT:172269","NEWT:9534","NEWT:2126348","NEWT:5180","NEWT:256737","NEWT:9541","NEWT:8694","NEWT:33936","NEWT:8692","NEWT:542","NEWT:2903","NEWT:185579","NEWT:872227","NEWT:13076","NEWT:2587410","NEWT:207340","NEWT:1006581","NEWT:8673","NEWT:33940","NEWT:2126337","NEWT:550","NEWT:33941","NEWT:554","NEWT:451516","NEWT:552","NEWT:1325291","NEWT:42410","NEWT:36185","NEWT:1054211","NEWT:1225786","NEWT:771870","NEWT:51338","NEWT:9995","NEWT:575412","NEWT:28112","NEWT:49012","NEWT:6493","NEWT:10832","NEWT:6494","NEWT:6491","NEWT:507601","NEWT:520","NEWT:64657","NEWT:186441","NEWT:643680","NEWT:214092","NCBITaxon:6157","NEWT:13095","NEWT:162425","NEWT:104105","NEWT:216257","NEWT:9986","NEWT:8654","NEWT:8658","NEWT:1268063","NEWT:8657","NEWT:9983","NEWT:8655","NEWT:51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