{"database":"Pride","file_versions":[{"headers":{"Content-Type":["application/json"]},"body":{"files":{"Txt":["ftp://ftp.pride.ebi.ac.uk/pride/data/archive/2026/04/PXD071548/checksum.txt"],"Msf":["ftp://ftp.pride.ebi.ac.uk/pride/data/archive/2026/04/PXD071548/PRF_Q_2021_D_RAY_673_51514.msf","ftp://ftp.pride.ebi.ac.uk/pride/data/archive/2026/04/PXD071548/PRF_A_2023_D_RAY_1098_63158_63173_1_8.msf"],"Raw":["ftp://ftp.pride.ebi.ac.uk/pride/data/archive/2026/04/PXD071548/PRF_A_2023_D_RAY_1098_63158_63173_6.raw","ftp://ftp.pride.ebi.ac.uk/pride/data/archive/2026/04/PXD071548/PRF_A_2023_D_RAY_1098_63158_63173_7.raw","ftp://ftp.pride.ebi.ac.uk/pride/data/archive/2026/04/PXD071548/PRF_Q_2021_D_RAY_673_51514.raw","ftp://ftp.pride.ebi.ac.uk/pride/data/archive/2026/04/PXD071548/PRF_A_2023_D_RAY_1098_63158_63173_5.raw","ftp://ftp.pride.ebi.ac.uk/pride/data/archive/2026/04/PXD071548/PRF_A_2023_D_RAY_1098_63158_63173_8.raw","ftp://ftp.pride.ebi.ac.uk/pride/data/archive/2026/04/PXD071548/PRF_A_2023_D_RAY_1098_63158_63173_2.raw","ftp://ftp.pride.ebi.ac.uk/pride/data/archive/2026/04/PXD071548/PRF_A_2023_D_RAY_1098_63158_63173_1.raw","ftp://ftp.pride.ebi.ac.uk/pride/data/archive/2026/04/PXD071548/PRF_A_2023_D_RAY_1098_63158_63173_3.raw","ftp://ftp.pride.ebi.ac.uk/pride/data/archive/2026/04/PXD071548/PRF_A_2023_D_RAY_1098_63158_63173_4.raw"]},"type":"primary"},"statusCode":"OK","statusCodeValue":200}],"scores":null,"additional":{"labhead_mail":["dipray@umich.edu"],"submitter":["Dipankar Ray"],"technology_type":["Mass Spectrometry","Bottom-up proteomics"],"disease":["Esophageal Adenosquamous Carcinoma"],"software":[""],"submitter_keywords":["H2ax","Homologous recombination repair (hrr)","Isgylation","Radioresistance","Esophageal adenocarcinoma."],"full_dataset_link":["https://www.ebi.ac.uk/pride/archive/projects/PXD071548"],"tissue":["Epithelial Cell"],"sample_protocol":["Mass spectrometry. Immunoprecipitated samples were separated on a polyacrylamide gel, and the gel was stained with colloidal Coomassie. In-gel digestion followed by identification of post-translationally modified sites was performed similarly as described previously (51). After trypsin digestion, peptides were resolved on a nano-capillary reverse phase column and eluent was directly introduced into Orbitrap Fusion tribrid mass spectrometer (Thermo Scientific, San Jose CA) using an EasySpray source.  MS1 scans were acquired at 120K resolution (AGC target=1x106; max IT=50 ms).  Data-dependent collision induced dissociation MS/MS spectra were acquired using Top speed method (3 seconds) following each MS1 scan (NCE ~32%; AGC target 1x105; max IT 45 ms).   Proteins were identified by searching for the data against UniProt H sapien protein database () using Proteome Discoverer (v3.0, Thermo Scientific).  Search parameters included MS1 mass tolerance of 10 ppm and fragment tolerance of 0.05 Da; two missed cleavages were allowed; carbamidimethylation of cysteine, oxidation of methionine, and deamidation of aspergine and glutamine, ubiquitin remnant (K-gg; +114.043 Da) on lysine were considered as potential modifications.  Percolator node of Proteome Discoverer was used to filter and retain high quality proteins/peptides. Spectral matches to ubiquitinated/ISGylated peptides were manually verified. Tandem Mass Tags (TMTpro). For our studies, we have purchased the TMTpro 16-plex kit from Invitrogen (Cat# A44520) and used it according to the manufacturer’s protocol. Briefly, we used Flo1 cells transfected either with control or ISG15 siRNAs and were then exposed to either sham or 4 Gy. Samples were collected 6h post-IR and equal (75 mg) amounts of proteins were labeled using specific isotopes using a multiplex TMT kit. Mass spectrometry was performed at the University of Michigan Proteomic Resource Facility using their optimized protocol.  Briefly, after trypsin digestion the samples were labeled with TMTpro reagents as per the manufacturer’s protocol.  After combining the TMT labeled samples, an offline fractionation into 8 fractions was performed using high pH reversed-phase peptide fractionation kit (Pierce; Cat #84868).  Fractions were dried and reconstituted in 9 ml.  Orbitrap Ascend Tribrid equipped with FAIMS source (Thermo Fisher Scientific) and Vanquish Neo UHPLC were used to acquire the data.  Two l of the sample was resolved on an Easy-Spray PepMap Neo column (75 m i.d. x 50 cm; Thermo Scientific) at the flow-rate of 300 nl/min using 0.1% formic acid/acetonitrile gradient system (3-19% acetonitrile in 72 min;19--29% acetonitrile in 28 min; 29-41% in 20 min followed by 10 min column wash at 95% acetonitrile and re-equilibration) and directly spray onto the mass spectrometer using EasySpray source (Thermo Fisher Scientific).  FAIMS source was operated in standard resolution mode, with a nitrogen gas flow of 4.2 L/min, and inner and outer electrode temperature of 100 °C and dispersion voltage or -5000 V.   Two compensation voltages (CVs) of -45 and -65 V, 1.5 seconds per CV, were employed to select ions that enter the mass spectrometer for MS1 scan and MS/MS cycles.   Mass spectrometer was set to collect MS1 scan (Orbitrap; 400-1600 m/z; 120K resolution; AGC target of 100%; max IT in Auto) following which precursor ions with charge states of 2-6 were isolated by quadrupole mass filter at 0.7 m/z width and fragmented by collision induced dissociation in ion trap (NCE 30%; normalized AGC target of 100%; max IT 35 ms).  For multinotch-MS3, the top 10 precursors from each MS2 were fragmented by HCD followed by Orbitrap analysis (NCE 55; 45K resolution; normalized AGC target of 200%; max IT 200 ms, 100-500 m/z scan range)."],"repository":["Pride"],"quantification_method":[""],"modification":[""],"data_protocol":["Proteome Discoverer (v3.0; Thermo Fisher) was used for data analysis.  MS2 spectra were searched against SwissProt human protein database (20347 entries; sp_canonical TaxID=9606 (v2023-03-01)) using the following search parameters: MS1 and MS2 tolerance were set to 10 ppm and 0.6 Da, respectively; carbamidomethylation of cysteines (57.02146 Da) and TMTpro labeling of lysine and N-termini of peptides were considered static modifications; oxidation of methionine (15.9949 Da) and deamidation of asparagine and glutamine (0.98401 Da) were considered variable.  Identified proteins and peptides were filtered to retain only those that passed ≤1% FDR threshold.  Quantitation was performed using high-quality MS3 spectra (Average signal-to-noise ratio of 10 and <60% isolation interference).  Cell lysates from three independent replicates were used and compared to identify reliable proteomic alterations (up and downregulated proteins) with statistical significance (p>0.05)."],"omics_type":["Proteomics"],"labhead":["Dipankar Ray"],"instrument_platform":[""],"labhead_affiliation":["Departments of Radiation Oncology, The University of Michigan Medical School, Ann Arbor, Michigan 48109."],"submission_type":["PARTIAL"],"species":["Homo Sapiens (human)"],"submitter_mail":["dipray@umich.edu"],"publication":["41812883 Ghosh A, Ray P, Thomas D, Jeeyar V, Pillai S, Basrur V, Bondarenko IV, Bellile E, Wang DH, Morgan MA, Zhang Q, Beer DG, Lagisetty KH, Lawrence TS, Ray D. ISGylation of γH2AX retains MDC1 and facilitates homologous recombination repair causing radioresistance in esophageal adenocarcinoma. J Biol Chem. 2026 302(5):111358 10.1016/j.jbc.2026.111358"],"submitter_affiliation":["University of Michigan"],"submitter_country":["United States"],"pubmed_abstract":["High expression of interferon-stimulated gene 15 (ISG15) has been associated with poor survival in patients with esophageal adenocarcinoma (EAC). Like ubiquitin, ISG15 utilizes its C-terminal LRGG motif to post-translationally modify target proteins through a process called ISGylation, thereby influencing their stability, function, and interaction networks. Given ISG15's role in the replication stress response, we hypothesized that it may also contribute to DNA repair mechanisms. We found that ISG15 is upregulated following ionizing radiation (IR), and its knockdown disrupts the IR-induced G2/M checkpoint, leading to increased radiosensitivity in EAC cells. In synchronized cells, ISG15 expression peaks during the S/G2 phases. Knockdown of ISG15 impairs homologous recombination repair (HRR) with compensatory upregulation of non-homologous end joining (NHEJ). Similarly, cells expressing an ISGylation-defective ISG15<sup>LRAA</sup> mutant exhibit reduced HRR activity and elevated NHEJ, highlighting the critical role of ISGylation in the DNA damage response (DDR). Further investigation revealed that IR-induced ISG15 modifies γH2AX at lysine 120 (K120). Overexpression of an H2AX<sup>K120R</sup> mutant in EAC cells resulted in diminished MDC1 retention at DNA damage sites, mirroring the phenotype observed with ISG15 knockdown. Additionally, depletion of ISG15 delays RAD51 foci formation at damage sites. Using a tissue microarray of chemoresistant EAC patients, we observed that ISG15 is expressed in almost all cases and, along with high RAD51 expression, correlates with poorer prognosis in node-positive patients. Collectively, we identify γH2AX as a novel substrate of IR-induced ISGylation, which facilitates efficient recruitment and retention of downstream HRR proteins and may contribute to radioresistance in EAC."],"pubmed_title":["ISGylation of γH2AX retains MDC1 and facilitates homologous recombination repair causing radioresistance in esophageal adenocarcinoma."],"pubmed_authors":["Ghosh Archismaan A, Ray Paramita P, Thomas Dafydd D, Jeeyar Vinay V, Pillai Shreya S, Basrur Venkatesha V, Bondarenko Irina V IV, Bellile Emily E, Wang David H DH, Morgan Meredith A MA, Zhang Qiang Q, Beer David G DG, Lagisetty Kiran H KH, Lawrence Theodore S TS, Ray Dipankar D"],"additional_accession":[]},"is_claimable":false,"name":"ISGylation of H2AX retains MDC1 and facilitates homologous recombination repair causing radioresistance in esophageal adenocarcinoma","description":"High expression of interferon-stimulated gene 15 (ISG15) has been associated with poor survival in patients with esophageal adenocarcinoma (EAC). Like ubiquitin, ISG15 utilizes its C-terminal LRGG motif to post-translationally modify target proteins through a process called ISGylation, thereby influencing their stability, function, and interaction networks. Given ISG15’s role in the replication stress response, we hypothesized that it may also contribute to DNA repair mechanisms. We found that ISG15 is upregulated following ionizing radiation (IR), and its knockdown disrupts the IR-induced G2/M checkpoint, leading to increased radiosensitivity in EAC cells. In synchronized cells, ISG15 expression peaks during the S/G2 phases. Knockdown of ISG15 impairs homologous recombination repair (HRR) with compensatory upregulation of non-homologous end joining (NHEJ). Similarly, cells expressing an ISGylation-defective ISG15LRAA mutant exhibit reduced HRR activity and elevated NHEJ, highlighting the critical role of ISGylation in the DNA damage response (DDR). Further investigation revealed that IR-induced ISG15 modifies H2AX at lysine 120 (K120). Overexpression of an H2AXK120R mutant in EAC cells resulted in diminished MDC1 retention at DNA damage sites, mirroring the phenotype observed with ISG15 knockdown. Additionally, depletion of ISG15 delays RAD51 foci formation at damage sites. Using a tissue microarray of chemoresistant EAC patients, we observed that ISG15 is expressed in almost all cases and that along with high RAD51 expression correlates with poorer prognosis in node-positive patients. Collectively, we identify H2AX as a novel substrate of IR-induced ISGylation, which facilitates efficient recruitment and retention of downstream HRR proteins and may contribute to radioresistance in 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