Epigenetic reprogramming of Runx3 reinforces CD8 + T-cell function and improves the clinical response to immunotherapy Article Swipe
Zongzhi Liu
,
Xiang Li
,
Yibo Gao
,
Jiejie Liu
,
Ya-Ting Feng
,
Liu Yang
,
Junyun Wang
,
Chunmeng Wang
,
Dongrui Wang
,
Jie He
,
Weidong Han
,
Qian Mei
,
Yingli Sun
·
YOU?
·
· 2023
· Open Access
·
· DOI: https://doi.org/10.1186/s12943-023-01768-0
YOU?
·
· 2023
· Open Access
·
· DOI: https://doi.org/10.1186/s12943-023-01768-0
Background Checkpoint blockade immunotherapy, represented by PD-1 or PD-L1 antibody treatment, has been of tremendous success in clinical practice. However, the low clinical response rate and lack of biomarkers for prediction of the immune response limit the clinical application of anti-PD-1 immunotherapy. Our recent work showed that a combination of low-dose decitabine and PD-1-ab significantly improved the complete response (CR) rate of cHL patients from 32 to 71%, which indicates that there is a significant correlation between epigenetic regulation and the clinical response to immunotherapy. Methods We recruited two groups of Hodgkin lymphoma patients who were treated with anti-PD-1 and DAC+anti-PD-1. CD8+ T cells were isolated from the patients' peripheral blood, DNA methylation was analyzed by EPIC, the expression profile was analyzed by RNA-seq, and multigroup analysis was performed with IPA and GSEA functional annotations. We explored the effect of DAC on the function of CD8+ T cells in the blood, spleen, tumor and lymph nodes using a mouse model. Furthermore, we explored the function of Tils in the tumor microenvironment. Then, we constructed Runx3-knockout mice to confirm the T-cell-specific function of Runx3 in CD8+ T cells and analyzed various subtypes of T cells and cytokines using mass cytometry (CyTOF). Results Multiomics analysis identified that DNA methylation reprogramming of Runx3 was a crucial mediator of CD8+ T-cell function. Multiomics data showed that reversal of methylation of the Runx3 promoter promoted the infiltration of CD8+ TILs and mitigated the exhaustion of CD8+ T cells. Furthermore, experiments on tissue-specific Runx3-knockout mice showed that Runx3 deficiency reduced CD8+ T infiltration and the differentiation of effector T and memory T cells. Furthermore, Runx3 deficiency significantly decreased CCR3 and CCR5 levels. Immunotherapy experiments in Runx3 conditional knockout mice showed that DAC could not reverse the resistance of anti-PD-1 in the absence of Runx3. Moreover, both our clinical data and data from TISIDB showed that Runx3 could be a potential biomarker for immunotherapy to predict the clinical response rate. Conclusion We demonstrate that the DNA methylation of Runx3 plays a critical role in CD8+ T-cell infiltration and differentiation during decitabine-primed PD-1-ab immunotherapy, which provides a supporting mechanism for the essential role of epiregulation in immunotherapy.
Related Topics
Concepts
Immunotherapy
CD8
Cancer research
Biology
DNA methylation
Reprogramming
Tumor microenvironment
Cytotoxic T cell
Immune checkpoint
Cancer immunotherapy
T cell
Epigenetics
Immune system
Decitabine
Immunology
Cell
Gene expression
Genetics
Gene
In vitro
Metadata
- Type
- article
- Language
- en
- Landing Page
- https://doi.org/10.1186/s12943-023-01768-0
- https://molecular-cancer.biomedcentral.com/counter/pdf/10.1186/s12943-023-01768-0
- OA Status
- gold
- Cited By
- 39
- References
- 57
- Related Works
- 10
- OpenAlex ID
- https://openalex.org/W4376641254
All OpenAlex metadata
Raw OpenAlex JSON
- OpenAlex ID
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https://openalex.org/W4376641254Canonical identifier for this work in OpenAlex
- DOI
-
https://doi.org/10.1186/s12943-023-01768-0Digital Object Identifier
- Title
-
Epigenetic reprogramming of Runx3 reinforces CD8 + T-cell function and improves the clinical response to immunotherapyWork title
- Type
-
articleOpenAlex work type
- Language
-
enPrimary language
- Publication year
-
2023Year of publication
- Publication date
-
2023-05-16Full publication date if available
- Authors
-
Zongzhi Liu, Xiang Li, Yibo Gao, Jiejie Liu, Ya-Ting Feng, Liu Yang, Junyun Wang, Chunmeng Wang, Dongrui Wang, Jie He, Weidong Han, Qian Mei, Yingli SunList of authors in order
- Landing page
-
https://doi.org/10.1186/s12943-023-01768-0Publisher landing page
- PDF URL
-
https://molecular-cancer.biomedcentral.com/counter/pdf/10.1186/s12943-023-01768-0Direct link to full text PDF
- Open access
-
YesWhether a free full text is available
- OA status
-
goldOpen access status per OpenAlex
- OA URL
-
https://molecular-cancer.biomedcentral.com/counter/pdf/10.1186/s12943-023-01768-0Direct OA link when available
- Concepts
-
Immunotherapy, CD8, Cancer research, Biology, DNA methylation, Reprogramming, Tumor microenvironment, Cytotoxic T cell, Immune checkpoint, Cancer immunotherapy, T cell, Epigenetics, Immune system, Decitabine, Immunology, Cell, Gene expression, Genetics, Gene, In vitroTop concepts (fields/topics) attached by OpenAlex
- Cited by
-
39Total citation count in OpenAlex
- Citations by year (recent)
-
2025: 19, 2024: 15, 2023: 5Per-year citation counts (last 5 years)
- References (count)
-
57Number of works referenced by this work
- Related works (count)
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10Other works algorithmically related by OpenAlex
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| abstract_inverted_index.data | 220, 303, 305 |
| abstract_inverted_index.from | 65, 107, 306 |
| abstract_inverted_index.lack | 27 |
| abstract_inverted_index.mass | 198 |
| abstract_inverted_index.mice | 176, 249, 283 |
| abstract_inverted_index.rate | 25, 61 |
| abstract_inverted_index.role | 336, 355 |
| abstract_inverted_index.that | 47, 71, 205, 222, 251, 285, 309, 327 |
| abstract_inverted_index.were | 96, 105 |
| abstract_inverted_index.with | 98, 130 |
| abstract_inverted_index.work | 45 |
| abstract_inverted_index.EPIC, | 117 |
| abstract_inverted_index.PD-L1 | 9 |
| abstract_inverted_index.Runx3 | 183, 210, 228, 252, 269, 280, 310, 332 |
| abstract_inverted_index.Then, | 172 |
| abstract_inverted_index.cells | 104, 148, 187, 194 |
| abstract_inverted_index.could | 287, 311 |
| abstract_inverted_index.limit | 36 |
| abstract_inverted_index.lymph | 155 |
| abstract_inverted_index.mouse | 159 |
| abstract_inverted_index.nodes | 156 |
| abstract_inverted_index.plays | 333 |
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| abstract_inverted_index.there | 72 |
| abstract_inverted_index.tumor | 153, 170 |
| abstract_inverted_index.using | 157, 197 |
| abstract_inverted_index.which | 69, 347 |
| abstract_inverted_index.Runx3. | 298 |
| abstract_inverted_index.T-cell | 217, 339 |
| abstract_inverted_index.TISIDB | 307 |
| abstract_inverted_index.blood, | 111, 151 |
| abstract_inverted_index.cells. | 243, 267 |
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| abstract_inverted_index.effect | 139 |
| abstract_inverted_index.groups | 90 |
| abstract_inverted_index.immune | 34 |
| abstract_inverted_index.memory | 265 |
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| abstract_inverted_index.Results | 201 |
| abstract_inverted_index.absence | 296 |
| abstract_inverted_index.between | 77 |
| abstract_inverted_index.confirm | 178 |
| abstract_inverted_index.crucial | 213 |
| abstract_inverted_index.levels. | 276 |
| abstract_inverted_index.predict | 319 |
| abstract_inverted_index.profile | 120 |
| abstract_inverted_index.reduced | 254 |
| abstract_inverted_index.reverse | 289 |
| abstract_inverted_index.spleen, | 152 |
| abstract_inverted_index.success | 16 |
| abstract_inverted_index.treated | 97 |
| abstract_inverted_index.various | 190 |
| abstract_inverted_index.(CyTOF). | 200 |
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| abstract_inverted_index.RNA-seq, | 124 |
| abstract_inverted_index.analysis | 127, 203 |
| abstract_inverted_index.analyzed | 115, 122, 189 |
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| abstract_inverted_index.blockade | 3 |
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| abstract_inverted_index.critical | 335 |
| abstract_inverted_index.effector | 262 |
| abstract_inverted_index.explored | 137, 163 |
| abstract_inverted_index.function | 144, 165, 181 |
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| abstract_inverted_index.reversal | 223 |
| abstract_inverted_index.subtypes | 191 |
| abstract_inverted_index.Moreover, | 299 |
| abstract_inverted_index.anti-PD-1 | 41, 99, 293 |
| abstract_inverted_index.biomarker | 315 |
| abstract_inverted_index.cytokines | 196 |
| abstract_inverted_index.cytometry | 199 |
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| abstract_inverted_index.essential | 354 |
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| abstract_inverted_index.potential | 314 |
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| abstract_inverted_index.recruited | 88 |
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| abstract_inverted_index.Checkpoint | 2 |
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| abstract_inverted_index.biomarkers | 29 |
| abstract_inverted_index.decitabine | 52 |
| abstract_inverted_index.deficiency | 253, 270 |
| abstract_inverted_index.epigenetic | 78 |
| abstract_inverted_index.exhaustion | 239 |
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| abstract_inverted_index.identified | 204 |
| abstract_inverted_index.multigroup | 126 |
| abstract_inverted_index.peripheral | 110 |
| abstract_inverted_index.prediction | 31 |
| abstract_inverted_index.regulation | 79 |
| abstract_inverted_index.resistance | 291 |
| abstract_inverted_index.supporting | 350 |
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| abstract_inverted_index.application | 39 |
| abstract_inverted_index.combination | 49 |
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| abstract_inverted_index.constructed | 174 |
| abstract_inverted_index.correlation | 76 |
| abstract_inverted_index.demonstrate | 326 |
| abstract_inverted_index.experiments | 245, 278 |
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| abstract_inverted_index.significant | 75 |
| abstract_inverted_index.Furthermore, | 161, 244, 268 |
| abstract_inverted_index.annotations. | 135 |
| abstract_inverted_index.infiltration | 232, 257, 340 |
| abstract_inverted_index.Immunotherapy | 277 |
| abstract_inverted_index.epiregulation | 357 |
| abstract_inverted_index.immunotherapy | 317 |
| abstract_inverted_index.reprogramming | 208 |
| abstract_inverted_index.significantly | 55, 271 |
| abstract_inverted_index.DAC+anti-PD-1. | 101 |
| abstract_inverted_index.Runx3-knockout | 175, 248 |
| abstract_inverted_index.immunotherapy, | 4, 346 |
| abstract_inverted_index.immunotherapy. | 42, 85, 359 |
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| abstract_inverted_index.tissue-specific | 247 |
| abstract_inverted_index.decitabine-primed | 344 |
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| corresponding_author_ids | https://openalex.org/A5101670425 |
| countries_distinct_count | 1 |
| institutions_distinct_count | 13 |
| corresponding_institution_ids | https://openalex.org/I76130692 |
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| sustainable_development_goals[0].display_name | Good health and well-being |
| citation_normalized_percentile.value | 0.98557142 |
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| citation_normalized_percentile.is_in_top_10_percent | True |