Deterministic reprogramming of neutrophils within tumors
Neutrophils are increasingly recognized as key players in the tumor immune response and are associated with poor clinical outcomes. Despite recent advances characterizing the diversity of neutrophil states in cancer, common trajectories and mechanisms governing the ontogeny and relationship between...
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| Veröffentlicht in: | Science (American Association for the Advancement of Science) Jg. 383; H. 6679; S. eadf6493 |
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| Hauptverfasser: | , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format: | Journal Article |
| Sprache: | Englisch |
| Veröffentlicht: |
United States
12.01.2024
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| ISSN: | 1095-9203, 1095-9203 |
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| Abstract | Neutrophils are increasingly recognized as key players in the tumor immune response and are associated with poor clinical outcomes. Despite recent advances characterizing the diversity of neutrophil states in cancer, common trajectories and mechanisms governing the ontogeny and relationship between these neutrophil states remain undefined. Here, we demonstrate that immature and mature neutrophils that enter tumors undergo irreversible epigenetic, transcriptional, and proteomic modifications to converge into a distinct, terminally differentiated dcTRAIL-R1
state. Reprogrammed dcTRAIL-R1
neutrophils predominantly localize to a glycolytic and hypoxic niche at the tumor core and exert pro-angiogenic function that favors tumor growth. We found similar trajectories in neutrophils across multiple tumor types and in humans, suggesting that targeting this program may provide a means of enhancing certain cancer immunotherapies. |
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| AbstractList | Neutrophils are increasingly recognized as key players in the tumor immune response and are associated with poor clinical outcomes. Despite recent advances characterizing the diversity of neutrophil states in cancer, common trajectories and mechanisms governing the ontogeny and relationship between these neutrophil states remain undefined. Here, we demonstrate that immature and mature neutrophils that enter tumors undergo irreversible epigenetic, transcriptional, and proteomic modifications to converge into a distinct, terminally differentiated dcTRAIL-R1+ state. Reprogrammed dcTRAIL-R1+ neutrophils predominantly localize to a glycolytic and hypoxic niche at the tumor core and exert pro-angiogenic function that favors tumor growth. We found similar trajectories in neutrophils across multiple tumor types and in humans, suggesting that targeting this program may provide a means of enhancing certain cancer immunotherapies.Neutrophils are increasingly recognized as key players in the tumor immune response and are associated with poor clinical outcomes. Despite recent advances characterizing the diversity of neutrophil states in cancer, common trajectories and mechanisms governing the ontogeny and relationship between these neutrophil states remain undefined. Here, we demonstrate that immature and mature neutrophils that enter tumors undergo irreversible epigenetic, transcriptional, and proteomic modifications to converge into a distinct, terminally differentiated dcTRAIL-R1+ state. Reprogrammed dcTRAIL-R1+ neutrophils predominantly localize to a glycolytic and hypoxic niche at the tumor core and exert pro-angiogenic function that favors tumor growth. We found similar trajectories in neutrophils across multiple tumor types and in humans, suggesting that targeting this program may provide a means of enhancing certain cancer immunotherapies. Neutrophils are increasingly recognized as key players in the tumor immune response and are associated with poor clinical outcomes. Despite recent advances characterizing the diversity of neutrophil states in cancer, common trajectories and mechanisms governing the ontogeny and relationship between these neutrophil states remain undefined. Here, we demonstrate that immature and mature neutrophils that enter tumors undergo irreversible epigenetic, transcriptional, and proteomic modifications to converge into a distinct, terminally differentiated dcTRAIL-R1 state. Reprogrammed dcTRAIL-R1 neutrophils predominantly localize to a glycolytic and hypoxic niche at the tumor core and exert pro-angiogenic function that favors tumor growth. We found similar trajectories in neutrophils across multiple tumor types and in humans, suggesting that targeting this program may provide a means of enhancing certain cancer immunotherapies. |
| Author | Caronni, Nicoletta Sharma, Ankur Moalli, Federica Angeli, Veronique Ng, Melissa S F Cheng, Hui Calvo, Gabriel F Zhang, Yuning Liong, Ka Hang Ballesteros, Iván Ng, Lai Guan Jin, Jingsi Narang, Vipin Bleriot, Camille Chong, Shu Zhen Duan, Kaibo Ginhoux, Florent Kwok, Immanuel Iannacone, Matteo Li, Mengwei Shen, Baiyong He, Rui Teh, Ye Chean Liu, Dehua Tan, Yingrou Tey, Hong Liang Ostuni, Renato Tan, Leonard Liu, Yingbin Hidalgo, Andrés Leong, Keith Cerezo-Wallis, Daniela Liu, Yao Shi, Changming Liu, Zhaoyuan Liu, Lianxin Jiang, Lingxi Chen, Jinmiao Loh, Yuin-Han Wu, Dandan Yang, Katharine Qi, Jingjing Cheng, Tao |
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Vascular Biology and Therapeutics Program and Department of Immunobiology, Yale University School of Medicine, New Haven, CT, USA – sequence: 6 givenname: Yingrou orcidid: 0000-0003-3563-6546 surname: Tan fullname: Tan, Yingrou organization: National Skin Centre, National Healthcare Group, Singapore – sequence: 7 givenname: Keith orcidid: 0000-0002-0568-3387 surname: Leong fullname: Leong, Keith organization: Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (ASTAR), Singapore – sequence: 8 givenname: Gabriel F orcidid: 0000-0002-3623-236X surname: Calvo fullname: Calvo, Gabriel F organization: Department of Mathematics & MOLAB-Mathematical Oncology Laboratory, University of Castilla-La Mancha, Ciudad Real, Spain – sequence: 9 givenname: Katharine orcidid: 0000-0002-8209-1289 surname: Yang fullname: Yang, Katharine organization: Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (ASTAR), Singapore – sequence: 10 givenname: Yuning surname: Zhang fullname: Zhang, Yuning organization: Immunology Program, Life Science Institute, National University of Singapore, Singapore – sequence: 11 givenname: Jingsi surname: Jin fullname: Jin, Jingsi organization: Shanghai Immune Therapy Institute, Renji Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China – sequence: 12 givenname: Ka Hang orcidid: 0000-0002-7575-032X surname: Liong fullname: Liong, Ka Hang organization: Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (ASTAR), Singapore – sequence: 13 givenname: Dandan surname: Wu fullname: Wu, Dandan organization: Shanghai Institute of Immunology, Shanghai Jiao Tong University School of Medicine, Shanghai, China – sequence: 14 givenname: Rui surname: He fullname: He, Rui organization: Shanghai Immune Therapy Institute, Renji Hospital, Shanghai Jiao Tong University School of Medicine, Shanghai, China – sequence: 15 givenname: Dehua orcidid: 0000-0002-7633-9006 surname: Liu fullname: Liu, Dehua organization: Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (ASTAR), Singapore – sequence: 16 givenname: Ye Chean orcidid: 0000-0003-0155-2109 surname: Teh fullname: Teh, Ye Chean organization: Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (ASTAR), Singapore – sequence: 17 givenname: Camille orcidid: 0000-0002-4298-2888 surname: Bleriot fullname: Bleriot, Camille organization: CNRS UMR8253, Institut Necker des Enfants Malades, Paris, France – sequence: 18 givenname: Nicoletta orcidid: 0000-0002-3263-7108 surname: Caronni fullname: Caronni, Nicoletta organization: Genomics of the Innate Immune System Unit, San Raffaele-Telethon Institute for Gene Therapy (SR-Tiget), IRCCS San Raffaele Scientific Institute, Milan, Italy – sequence: 19 givenname: Zhaoyuan orcidid: 0000-0002-3117-0833 surname: Liu fullname: Liu, Zhaoyuan organization: Shanghai Institute of Immunology, Shanghai Jiao Tong University School of Medicine, Shanghai, China – sequence: 20 givenname: Kaibo surname: Duan fullname: Duan, Kaibo organization: Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (ASTAR), Singapore – sequence: 21 givenname: Vipin surname: Narang fullname: Narang, Vipin organization: Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (ASTAR), Singapore – sequence: 22 givenname: Iván orcidid: 0000-0002-6246-2353 surname: Ballesteros fullname: Ballesteros, Iván organization: Area of Cell & Developmental Biology, Centro Nacional de Investigaciones Cardiovasculares Carlos III, Madrid, Spain – sequence: 23 givenname: Federica surname: Moalli fullname: Moalli, Federica organization: Experimental Imaging Centre, IRCCS San Raffaele Scientific Institute, Milan, Italy – sequence: 24 givenname: Mengwei surname: Li fullname: Li, Mengwei organization: Singapore Immunology Network (SIgN), Agency for Science, Technology and Research (ASTAR), 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Hematology & Blood Diseases Hospital, Chinese Academy of Medical Sciences & Peking Union Medical College, Tianjin, China – sequence: 33 givenname: Tao orcidid: 0000-0002-5925-2769 surname: Cheng fullname: Cheng, Tao organization: State Key Laboratory of Experimental Hematology, National Clinical Research Center for Blood Diseases, Haihe Laboratory of Cell Ecosystem, Institute of Hematology & Blood Diseases Hospital, Chinese Academy of Medical Sciences & Peking Union Medical College, Tianjin, China – sequence: 34 givenname: Veronique orcidid: 0000-0002-2759-3497 surname: Angeli fullname: Angeli, Veronique organization: Immunology Program, Life Science Institute, National University of Singapore, Singapore – sequence: 35 givenname: Ankur orcidid: 0000-0002-6862-136X surname: Sharma fullname: Sharma, Ankur organization: Curtin Health Innovation Research Institute, Curtin University, Bentley, Western Australia, Australia – sequence: 36 givenname: Yuin-Han orcidid: 0000-0002-4715-6454 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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/38207030$$D View this record in MEDLINE/PubMed |
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| SubjectTerms | Cellular Reprogramming - genetics Cellular Reprogramming - immunology Epigenesis, Genetic Humans Hypoxia Neoplasms - blood supply Neoplasms - immunology Neovascularization, Pathologic - genetics Neovascularization, Pathologic - immunology Neutrophils - immunology Proteomics Receptors, TNF-Related Apoptosis-Inducing Ligand - immunology Transcription, Genetic |
| Title | Deterministic reprogramming of neutrophils within tumors |
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