{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,15]],"date-time":"2026-10-15T00:45:02Z","timestamp":1792025102455,"version":"4.4.0"},"reference-count":52,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2022,1,12]],"date-time":"2022-01-12T00:00:00Z","timestamp":1641945600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2022,1,12]],"date-time":"2022-01-12T00:00:00Z","timestamp":1641945600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"DOI":"10.13039\/501100001809","name":"National Natural Science Foundation of China","doi-asserted-by":"publisher","award":["#8202290021"],"award-info":[{"award-number":["#8202290021"]}],"id":[{"id":"10.13039\/501100001809","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100003995","name":"Natural Science Foundation of Anhui Province","doi-asserted-by":"publisher","award":["#2008085J35,1908085MH281"],"award-info":[{"award-number":["#2008085J35,1908085MH281"]}],"id":[{"id":"10.13039\/501100003995","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Nat Commun"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>A complete diagnostic autopsy is the gold-standard to gain insight into Coronavirus disease 2019 (COVID-19) pathogenesis. To delineate the in situ immune responses to SARS-CoV-2 viral infection, here we perform comprehensive high-dimensional transcriptional and spatial immune profiling in 22 COVID-19 decedents from Wuhan, China. We find TIM-3-mediated and PD-1-mediated immunosuppression as a hallmark of severe COVID-19, particularly in men, with PD-1<jats:sup>+<\/jats:sup> cells being proximal rather than distal to TIM-3<jats:sup>+<\/jats:sup> cells. Concurrently, lymphocytes are distal, while activated myeloid cells are proximal, to SARS-CoV-2 viral antigens, consistent with prevalent SARS-CoV-2 infection of myeloid cells in multiple organs. Finally, viral load positively correlates with specific immunosuppression and dendritic cell markers. In summary, our data show that SARS-CoV-2 viral infection induces lymphocyte suppression yet myeloid activation in severe COVID-19, so these two cell types likely have distinct functions in severe COVID-19 disease progression, and should be targeted differently for therapy.<\/jats:p>","DOI":"10.1038\/s41467-021-27723-5","type":"journal-article","created":{"date-parts":[[2022,1,12]],"date-time":"2022-01-12T11:02:59Z","timestamp":1641985379000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":25,"title":["Postmortem high-dimensional immune profiling of severe COVID-19 patients reveals distinct patterns of immunosuppression and immunoactivation"],"prefix":"10.1038","volume":"13","author":[{"given":"Haibo","family":"Wu","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peiqi","family":"He","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yong","family":"Ren","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shiqi","family":"Xiao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wei","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhenbang","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Heng","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhe","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dingyu","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jun","family":"Cai","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiangdong","family":"Zhou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dongpo","family":"Jiang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Xiaochun","family":"Fei","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lei","family":"Zhao","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Heng","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhenhua","family":"Liu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rong","family":"Chen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Weiqing","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chaofu","family":"Wang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shuyang","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jiwei","family":"Qin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7587-9935","authenticated-orcid":false,"given":"Bj\u00f6rn","family":"Nashan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-8799-7426","authenticated-orcid":false,"given":"Cheng","family":"Sun","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2022,1,12]]},"reference":[{"key":"27723_CR1","doi-asserted-by":"publisher","first-page":"2620","DOI":"10.1172\/JCI137244","volume":"130","author":"G Chen","year":"2020","unstructured":"Chen, G. et al. Clinical and immunological features of severe and moderate coronavirus disease 2019. J. Clin. Investig. 130, 2620\u20132629 (2020).","journal-title":"J. Clin. Investig."},{"key":"27723_CR2","doi-asserted-by":"crossref","unstructured":"Chen Z., John Wherry E. T cell responses in patients with COVID-19. Nat. Rev. Immunol. 20, 529\u2013536 (2020).","DOI":"10.1038\/s41577-020-0402-6"},{"key":"27723_CR3","doi-asserted-by":"publisher","first-page":"1472","DOI":"10.3390\/jcm9051472","volume":"9","author":"M Salerno","year":"2020","unstructured":"Salerno, M. et al. No autopsies on COVID-19 deaths: a missed opportunity and the lockdown of science. J. Clin. Med. 9, 1472 (2020).","journal-title":"J. Clin. Med."},{"key":"27723_CR4","doi-asserted-by":"publisher","unstructured":"Xiong Q. et al. Single-cell immune profiling of matched disease and recovery phase blood of COVID-19 patients reveals anti-LAG3 based immune checkpoint therapy as a promising option. https:\/\/doi.org\/10.21203\/rs.3.rs-24576\/v1 (2020).","DOI":"10.21203\/rs.3.rs-24576\/v1"},{"key":"27723_CR5","doi-asserted-by":"crossref","unstructured":"Westmeier J. et al. Impaired Cytotoxic CD8(+) T cell response in elderly COVID-19 patients. mBio 11, e02243\u201320 (2020).","DOI":"10.1128\/mBio.02805-20"},{"key":"27723_CR6","doi-asserted-by":"publisher","first-page":"541","DOI":"10.1038\/s41423-020-0401-3","volume":"17","author":"HY Zheng","year":"2020","unstructured":"Zheng, H. Y. et al. Elevated exhaustion levels and reduced functional diversity of T cells in peripheral blood may predict severe progression in COVID-19 patients. Cell Mol. Immunol. 17, 541\u2013543 (2020).","journal-title":"Cell Mol. Immunol."},{"key":"27723_CR7","doi-asserted-by":"publisher","first-page":"e1008520","DOI":"10.1371\/journal.ppat.1008520","volume":"16","author":"Y Meng","year":"2020","unstructured":"Meng, Y. et al. Sex-specific clinical characteristics and prognosis of coronavirus disease-19 infection in Wuhan, China: a retrospective study of 168 severe patients. PLOS Pathog. 16, e1008520 (2020).","journal-title":"PLOS Pathog."},{"key":"27723_CR8","doi-asserted-by":"publisher","first-page":"2052","DOI":"10.1001\/jama.2020.6775","volume":"323","author":"S Richardson","year":"2020","unstructured":"Richardson, S. et al. Presenting characteristics, comorbidities, and outcomes among 5700 patients hospitalized With COVID-19 in the New York city area. JAMA 323, 2052\u20132059 (2020).","journal-title":"JAMA"},{"key":"27723_CR9","doi-asserted-by":"publisher","first-page":"442","DOI":"10.1038\/s41577-020-0348-8","volume":"20","author":"EP Scully","year":"2020","unstructured":"Scully, E. P., Haverfield, J., Ursin, R. L., Tannenbaum, C. & Klein, S. L. Considering how biological sex impacts immune responses and COVID-19 outcomes. Nat. Rev. Immunol. 20, 442\u2013447 (2020).","journal-title":"Nat. Rev. Immunol."},{"key":"27723_CR10","doi-asserted-by":"publisher","first-page":"626","DOI":"10.1038\/nri.2016.90","volume":"16","author":"SL Klein","year":"2016","unstructured":"Klein, S. L. & Flanagan, K. L. Sex differences in immune responses. Nat. Rev. Immunol. 16, 626\u2013638 (2016).","journal-title":"Nat. Rev. Immunol."},{"key":"27723_CR11","doi-asserted-by":"crossref","unstructured":"Demaria O. et al. Identification of druggable inhibitory immune checkpoints on Natural Killer cells in COVID-19. Cell. Mol. Immunol. 17, 995\u2013997 (2020).","DOI":"10.1038\/s41423-020-0493-9"},{"key":"27723_CR12","doi-asserted-by":"crossref","unstructured":"Mathew D. et al. Deep immune profiling of COVID-19 patients reveals distinct immunotypes with therapeutic implications. Science 369, eabc8511 (2020).","DOI":"10.1126\/science.369.6508.1203-l"},{"key":"27723_CR13","unstructured":"Sekine T. et al. Robust T cell immunity in convalescent individuals with asymptomatic or mild COVID-19. bioRxiv 183, 158\u2013168.e14. 2020.2006.2029.174888 (2020)."},{"key":"27723_CR14","doi-asserted-by":"crossref","unstructured":"Wilk A. J. et al. A single-cell atlas of the peripheral immune response to severe COVID-19. medRxiv 26, 1070\u20131076. 2020.2004.2017.20069930 (2020).","DOI":"10.1038\/s41591-020-0944-y"},{"key":"27723_CR15","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-020-17292-4","volume":"11","author":"S De Biasi","year":"2020","unstructured":"De Biasi, S. et al. Marked T cell activation, senescence, exhaustion and skewing towards TH17 in patients with COVID-19 pneumonia. Nat. Commun. 11, 3434 (2020).","journal-title":"Nat. Commun."},{"key":"27723_CR16","doi-asserted-by":"publisher","first-page":"442","DOI":"10.1016\/j.immuni.2020.06.024","volume":"53","author":"C Schultheiss","year":"2020","unstructured":"Schultheiss, C. et al. Next-generation sequencing of T and B cell receptor repertoires from COVID-19 patients showed signatures associated with severity of disease. Immunity 53, 442\u2013455 e444 (2020).","journal-title":"Immunity"},{"key":"27723_CR17","doi-asserted-by":"publisher","first-page":"842","DOI":"10.1038\/s41591-020-0901-9","volume":"26","author":"M Liao","year":"2020","unstructured":"Liao, M. et al. Single-cell landscape of bronchoalveolar immune cells in patients with COVID-19. Nat. Med. 26, 842\u2013844 (2020).","journal-title":"Nat. Med."},{"key":"27723_CR18","doi-asserted-by":"publisher","first-page":"313","DOI":"10.1016\/j.ijid.2020.05.106","volume":"97","author":"CK Kang","year":"2020","unstructured":"Kang, C. K. et al. Aberrant hyperactivation of cytotoxic T-cell as a potential determinant of COVID-19 severity. Int. J. Infect. Dis. 97, 313\u2013321 (2020).","journal-title":"Int. J. Infect. Dis."},{"key":"27723_CR19","doi-asserted-by":"publisher","first-page":"420","DOI":"10.1016\/S2213-2600(20)30076-X","volume":"8","author":"Z Xu","year":"2020","unstructured":"Xu, Z. et al. Pathological findings of COVID-19 associated with acute respiratory distress syndrome. Lancet Respiratory Med. 8, 420\u2013422 (2020).","journal-title":"Lancet Respiratory Med."},{"key":"27723_CR20","doi-asserted-by":"publisher","first-page":"e83","DOI":"10.1016\/j.jtho.2020.03.021","volume":"15","author":"L Bonomi","year":"2020","unstructured":"Bonomi, L., Ghilardi, L., Arnoldi, E., Tondini, C. A. & Bettini, A. C. A rapid fatal evolution of coronavirus disease-19 in a patient with advanced lung cancer with a long-time response to nivolumab. J. Thorac. Oncol. 15, e83\u2013e85 (2020).","journal-title":"J. Thorac. Oncol."},{"key":"27723_CR21","doi-asserted-by":"publisher","unstructured":"Lovly C. M. et al. Rapidly fatal pneumonitis from immunotherapy and concurrent SARS-CoV-2 infection in a patient with newly diagnosed lung cancer. medRxiv https:\/\/doi.org\/10.1101\/2020.04.29.20085738 (2020).","DOI":"10.1101\/2020.04.29.20085738"},{"key":"27723_CR22","doi-asserted-by":"crossref","first-page":"783","DOI":"10.1158\/2159-8290.CD-20-0422","volume":"10","author":"M Dai","year":"2020","unstructured":"Dai, M. et al. Patients with cancer appear more vulnerable to SARS-CoV-2: a multicenter study during the COVID-19 outbreak. Cancer Disco. 10, 783\u2013791 (2020).","journal-title":"Cancer Disco."},{"key":"27723_CR23","doi-asserted-by":"publisher","first-page":"870","DOI":"10.1016\/j.chom.2020.05.008","volume":"27","author":"A Park","year":"2020","unstructured":"Park, A. & Iwasaki, A. Type I and Type III interferons - induction, signaling, evasion, and application to combat COVID-19. Cell Host Microbe 27, 870\u2013878 (2020).","journal-title":"Cell Host Microbe"},{"key":"27723_CR24","doi-asserted-by":"publisher","first-page":"497","DOI":"10.1016\/S0140-6736(20)30183-5","volume":"395","author":"C Huang","year":"2020","unstructured":"Huang, C. et al. Clinical features of patients infected with 2019 novel coronavirus in Wuhan, China. Lancet 395, 497\u2013506 (2020).","journal-title":"Lancet"},{"key":"27723_CR25","doi-asserted-by":"publisher","first-page":"17","DOI":"10.1002\/JLB.3COVR0520-272R","volume":"108","author":"J Wang","year":"2020","unstructured":"Wang, J., Jiang, M., Chen, X. & Montaner, L. J. Cytokine storm and leukocyte changes in mild versus severe SARS-CoV-2 infection: review of 3939 COVID-19 patients in China and emerging pathogenesis and therapy concepts. J. Leukoc. Biol. 108, 17\u201341 (2020).","journal-title":"J. Leukoc. Biol."},{"key":"27723_CR26","doi-asserted-by":"crossref","unstructured":"Sanchez-Cerrillo I., et al. COVID-19 severity associates with pulmonary redistribution of CD1c+ DC and inflammatory transitional and nonclassical monocytes. J. Clin. Invest. 130, 6290\u20136300 (2020).","DOI":"10.1172\/JCI140335"},{"key":"27723_CR27","doi-asserted-by":"crossref","unstructured":"Peruzzi B. et al. Quantitative and qualitative alterations of circulating myeloid cells and plasmacytoid DC in SARS-CoV-2 infection. Immunology, 161, 345\u2013353 (2020).","DOI":"10.1111\/imm.13254"},{"key":"27723_CR28","doi-asserted-by":"crossref","unstructured":"Liang Y. et al. Highlight of immune pathogenic response and hematopathologic effect in SARS-CoV, MERS-CoV, and SARS-Cov-2 infection. Front. Immunol. 11, 1022 (2020).","DOI":"10.3389\/fimmu.2020.01022"},{"key":"27723_CR29","doi-asserted-by":"publisher","unstructured":"Chen Y. et al. The novel severe acute respiratory syndrome coronavirus 2 (SARS-CoV-2) directly decimates human spleens and lymph nodes. medRxiv, https:\/\/doi.org\/10.1101\/2020.03.27.20045427 (2020).","DOI":"10.1101\/2020.03.27.20045427"},{"key":"27723_CR30","doi-asserted-by":"publisher","first-page":"118102","DOI":"10.1016\/j.lfs.2020.118102","volume":"257","author":"A Jafarzadeh","year":"2020","unstructured":"Jafarzadeh, A., Chauhan, P., Saha, B., Jafarzadeh, S. & Nemati, M. Contribution of monocytes and macrophages to the local tissue inflammation and cytokine storm in COVID-19: Lessons from SARS and MERS, and potential therapeutic interventions. Life Sci. 257, 118102\u2013118102 (2020).","journal-title":"Life Sci."},{"key":"27723_CR31","doi-asserted-by":"crossref","unstructured":"Campana P. et al. Dendritic cells and SARS-CoV-2 infection: still an unclarified connection. Cells 9, 2046 (2020).","DOI":"10.3390\/cells9092046"},{"key":"27723_CR32","doi-asserted-by":"crossref","unstructured":"Wang C. et al. Alveolar macrophage dysfunction and cytokine storm in the pathogenesis of two severe COVID-19 patients. EBioMedicine 57, 102833 (2020).","DOI":"10.1016\/j.ebiom.2020.102833"},{"key":"27723_CR33","unstructured":"Yao, X. H. et al. [A pathological report of three COVID-19 cases by minimal invasive autopsies]. Zhonghua Bing Li Xue Za Zhi 49, 411\u2013417 (2020)."},{"key":"27723_CR34","doi-asserted-by":"publisher","unstructured":"Barton L., Duval E., Stroberg E., Ghosh S., Mukhopadhyay S. COVID-19 Autopsies, Oklahoma, USA. Am. J Clin. Pathol. 153 https:\/\/doi.org\/10.1093\/ajcp\/aqaa062 (2020).","DOI":"10.1093\/ajcp\/aqaa062"},{"key":"27723_CR35","doi-asserted-by":"crossref","unstructured":"Zhang Y., Gao Y., Qiao L., Wang W., Chen D. Inflammatory response cells during acute respiratory distress syndrome in patients with coronavirus disease 2019 (COVID-19). Ann. Intern. Med. 173, 402\u2013404 (2020).","DOI":"10.7326\/L20-0227"},{"key":"27723_CR36","doi-asserted-by":"publisher","first-page":"107233","DOI":"10.1016\/j.carpath.2020.107233","volume":"48","author":"LM Buja","year":"2020","unstructured":"Buja, L. M. et al. The emerging spectrum of cardiopulmonary pathology of the coronavirus disease 2019 (COVID-19): report of 3 autopsies from Houston, Texas, and review of autopsy findings from other United States cities. Cardiovasc Pathol. 48, 107233 (2020).","journal-title":"Cardiovasc Pathol."},{"key":"27723_CR37","doi-asserted-by":"publisher","unstructured":"Carsana L. et al. Pulmonary post-mortem findings in a series of COVID-19 cases from northern Italy: a two-centre descriptive study. Lancet Infect Dis https:\/\/doi.org\/10.1016\/S1473-3099(20)30434-5 (2020).","DOI":"10.1016\/S1473-3099(20)30434-5"},{"key":"27723_CR38","doi-asserted-by":"crossref","unstructured":"Adachi T. et al. Clinicopathologic and immunohistochemical findings from autopsy of patient with COVID-19, Japan. Emerg Infect Dis 26, 2157\u20132161 (2020).","DOI":"10.3201\/eid2609.201353"},{"key":"27723_CR39","doi-asserted-by":"publisher","first-page":"1419","DOI":"10.1016\/j.cell.2020.08.001","volume":"182","author":"J Schulte-Schrepping","year":"2020","unstructured":"Schulte-Schrepping, J. et al. Severe COVID-19 is marked by a dysregulated myeloid cell compartment. Cell 182, 1419\u20131440.e1423 (2020).","journal-title":"Cell"},{"key":"27723_CR40","doi-asserted-by":"publisher","unstructured":"Zhang D. et al. COVID-19 infection induces readily detectable morphological and inflammation-related phenotypic changes in peripheral blood monocytes, the severity of which correlate with patient outcome. medRxiv, https:\/\/doi.org\/10.1101\/2020.03.24.20042655 (2020).","DOI":"10.1101\/2020.03.24.20042655"},{"key":"27723_CR41","doi-asserted-by":"publisher","first-page":"281","DOI":"10.1016\/j.cell.2020.02.058","volume":"181","author":"AC Walls","year":"2020","unstructured":"Walls, A. C. et al. Structure, function, and antigenicity of the SARS-CoV-2 spike glycoprotein. Cell 181, 281\u2013292 e286 (2020).","journal-title":"Cell"},{"key":"27723_CR42","doi-asserted-by":"crossref","unstructured":"Martinez F. O., Combes T. W., Orsenigo F., Gordon S. Monocyte activation in systemic Covid-19 infection: assay and rationale. E. Bio. Medicine 59, 102964 (2020).","DOI":"10.1016\/j.ebiom.2020.102964"},{"key":"27723_CR43","doi-asserted-by":"publisher","first-page":"239","DOI":"10.1136\/jclinpath-2020-206522","volume":"73","author":"B Hanley","year":"2020","unstructured":"Hanley, B., Lucas, S. B., Youd, E., Swift, B. & Osborn, M. Autopsy in suspected COVID-19 cases. J. Clin. Pathol. 73, 239 (2020).","journal-title":"J. Clin. Pathol."},{"key":"27723_CR44","doi-asserted-by":"publisher","first-page":"1650","DOI":"10.1038\/nprot.2016.095","volume":"11","author":"M Pertea","year":"2016","unstructured":"Pertea, M., Kim, D., Pertea, G. M., Leek, J. T. & Salzberg, S. L. Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat. Protoc. 11, 1650\u20131667 (2016).","journal-title":"Nat. Protoc."},{"key":"27723_CR45","doi-asserted-by":"publisher","first-page":"1311","DOI":"10.1038\/s41374-020-0424-5","volume":"100","author":"S Gupta","year":"2020","unstructured":"Gupta, S., Zugazagoitia, J., Martinez-Morilla, S., Fuhrman, K. & Rimm, D. L. Digital quantitative assessment of PD-L1 using digital spatial profiling. Lab. Investig. 100, 1311\u20131317 (2020).","journal-title":"Lab. Investig."},{"key":"27723_CR46","doi-asserted-by":"publisher","first-page":"586","DOI":"10.1038\/s41587-020-0472-9","volume":"38","author":"CR Merritt","year":"2020","unstructured":"Merritt, C. R. et al. Multiplex digital spatial profiling of proteins and RNA in fixed tissue. Nat. Biotechnol. 38, 586\u2013599 (2020).","journal-title":"Nat. Biotechnol."},{"key":"27723_CR47","doi-asserted-by":"publisher","first-page":"563","DOI":"10.1007\/978-1-4939-9773-2_25","volume":"2055","author":"JM Beechem","year":"2020","unstructured":"Beechem, J. M. High-plex spatially resolved RNA and protein detection using digital spatial profiling: a technology designed for immuno-oncology biomarker discovery and translational research. Methods Mol. Biol. 2055, 563\u2013583 (2020).","journal-title":"Methods Mol. Biol."},{"key":"27723_CR48","doi-asserted-by":"publisher","first-page":"5503","DOI":"10.1158\/1078-0432.CCR-19-0104","volume":"25","author":"MI Toki","year":"2019","unstructured":"Toki, M. I. et al. High-plex predictive marker discovery for melanoma immunotherapy-treated patients using digital spatial profiling. Clin. Cancer Res.: Off. J. Am. Assoc. Cancer Res. 25, 5503\u20135512 (2019).","journal-title":"Clin. Cancer Res.: Off. J. Am. Assoc. Cancer Res."},{"key":"27723_CR49","doi-asserted-by":"crossref","unstructured":"Beasley G. M. et al. Dissecting the immune landscape of tumor draining lymph nodes in melanoma with high-plex spatially resolved protein detection. Cancer Immunol. Immunother. 70, 475\u2013483 (2020).","DOI":"10.1007\/s00262-020-02698-2"},{"key":"27723_CR50","doi-asserted-by":"publisher","first-page":"168","DOI":"10.1002\/hep.30347","volume":"70","author":"H Sun","year":"2019","unstructured":"Sun, H. et al. Human CD96 correlates to natural killer cell exhaustion and predicts the prognosis of human hepatocellular carcinoma. Hepatology 70, 168\u2013183 (2019).","journal-title":"Hepatology"},{"key":"27723_CR51","doi-asserted-by":"publisher","DOI":"10.1038\/s41467-018-03584-3","volume":"9","author":"C Sun","year":"2018","unstructured":"Sun, C. et al. Oncofetal gene SALL4 reactivation by hepatitis B virus counteracts miR-200c in PD-L1-induced T cell exhaustion. Nat. Commun. 9, 1241 (2018).","journal-title":"Nat. Commun."},{"key":"27723_CR52","doi-asserted-by":"publisher","first-page":"1535","DOI":"10.1158\/2326-6066.CIR-18-0757","volume":"7","author":"H Sun","year":"2019","unstructured":"Sun, H. et al. Accumulation of tumor-infiltrating CD49a(+) NK cells correlates with poor prognosis for human hepatocellular carcinoma. Cancer Immunol. Res. 7, 1535\u20131546 (2019).","journal-title":"Cancer Immunol. Res."}],"container-title":["Nature Communications"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41467-021-27723-5.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41467-021-27723-5","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41467-021-27723-5.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,11,24]],"date-time":"2022-11-24T15:46:29Z","timestamp":1669304789000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41467-021-27723-5"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,1,12]]},"references-count":52,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2022,12]]}},"alternative-id":["27723"],"URL":"https:\/\/doi.org\/10.1038\/s41467-021-27723-5","relation":{},"ISSN":["2041-1723"],"issn-type":[{"value":"2041-1723","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,1,12]]},"assertion":[{"value":"23 October 2020","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"1 December 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"12 January 2022","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"269"}}