Loss of Y in regulatory T lymphocytes in the tumor micro-environment of primary colorectal cancers and liver metastases.

Humans Colorectal Neoplasms / pathology Tumor Microenvironment / immunology T-Lymphocytes, Regulatory / immunology Male Liver Neoplasms / immunology Aged Programmed Cell Death 1 Receptor / metabolism Middle Aged Receptors, Immunologic / metabolism Female Lymphocytes, Tumor-Infiltrating / immunology Ikaros Transcription Factor / genetics

Journal

Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288

Informations de publication

Date de publication:
24 Apr 2024
Historique:
received: 24 08 2023
accepted: 18 04 2024
medline: 25 4 2024
pubmed: 25 4 2024
entrez: 24 4 2024
Statut: epublish

Résumé

Male sex is a risk factor for colorectal cancer (CRC) with higher illness burden and earlier onset. Thus, we hypothesized that loss of chromosome Y (LOY) in the tumor micro-environment (TME) might be involved in oncogenesis. Previous studies show that LOY in circulating leukocytes of aging men was associated with shorter survival and non-hematological cancer, as well as higher LOY in CD4 + T-lymphocytes in men with prostate cancer vs. controls. However, nothing is known about LOY in leukocytes infiltrating TME and we address this aspect here. We studied frequency and functional effects of LOY in blood, TME and non-tumorous tissue. Regulatory T-lymphocytes (Tregs) in TME had the highest frequency of LOY (22%) in comparison to CD4 + T-lymphocytes and cytotoxic CD8 + T-lymphocytes. LOY score using scRNA-seq was also linked to higher expression of PDCD1, TIGIT and IKZF2 in Tregs. PDCD1 and TIGIT encode immune checkpoint receptors involved in the regulation of Tregs function. Our study sets the direction for further functional research regarding a probable role of LOY in intensifying features related to the suppressive phenotype of Tregs in TME and consequently a possible influence on immunotherapy response in CRC patients.

Identifiants

DOI: 10.1038/s41598-024-60049-y PMID: 38658633
pubmed: 38658633
doi: 10.1038/s41598-024-60049-y
pii: 10.1038/s41598-024-60049-y
doi:

Substances chimiques

Programmed Cell Death 1 Receptor 0
TIGIT protein, human 0
Receptors, Immunologic 0
PDCD1 protein, human 0
Ikaros Transcription Factor 148971-36-2

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

9458

Subventions

Organisme : Fundacja na rzecz Nauki Polskiej
ID : MAB/2018 /6
Organisme : Hjärt-Lungfonden
ID : grant number 20210051
Organisme : Swedish Research Council
ID : 2020-02010

Informations de copyright

© 2024. The Author(s).

Références

Sung, H. et al. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 71, 209–249. https://doi.org/10.3322/caac.21660 (2021).
doi: 10.3322/caac.21660 pubmed: 33538338
Price, T. J. et al. Does the primary site of colorectal cancer impact outcomes for patients with metastatic disease?. Cancer 121, 830–835. https://doi.org/10.1002/cncr.29129 (2015).
doi: 10.1002/cncr.29129 pubmed: 25377235
Zhou, H. et al. Colorectal liver metastasis: Molecular mechanism and interventional therapy. Signal Transd. Target. Ther. 7, 70. https://doi.org/10.1038/s41392-022-00922-2 (2022).
doi: 10.1038/s41392-022-00922-2
Abancens, M., Bustos, V., Harvey, H., McBryan, J. & Harvey, B. J. Sexual dimorphism in colon cancer. Front. Oncol. https://doi.org/10.3389/fonc.2020.607909 (2020).
doi: 10.3389/fonc.2020.607909 pubmed: 33363037 pmcid: 7759153
Huyghe, J. R. et al. Discovery of common and rare genetic risk variants for colorectal cancer. Nat. Genet. 51, 76–87. https://doi.org/10.1038/s41588-018-0286-6 (2019).
doi: 10.1038/s41588-018-0286-6 pubmed: 30510241
Forsberg, L. A. et al. Mosaic loss of chromosome Y in peripheral blood is associated with shorter survival and higher risk of cancer. Nat. Genet. 46, 624–628. https://doi.org/10.1038/ng.2966 (2014).
doi: 10.1038/ng.2966 pubmed: 24777449 pmcid: 5536222
Thompson, D. et al. Genetic predisposition to mosaic Y chromosome loss in blood. Nature 575, 652–657 (2019).
doi: 10.1038/s41586-019-1765-3 pubmed: 31748747 pmcid: 6887549
Forsberg, L. et al. Mosaic loss of chromosome Y (LOY) in leukocytes matters. Nat. Genet. 51, 4–7. https://doi.org/10.1038/s41588-018-0267-9 (2019).
doi: 10.1038/s41588-018-0267-9 pubmed: 30374072
Dumanski, J. et al. Immune cells lacking Y chromosome show dysregulation of autosomal gene expression. Cell. Mol. Life Sci. 78, 4019–4033. https://doi.org/10.1007/s00018-021-03822-w (2021).
doi: 10.1007/s00018-021-03822-w pubmed: 33837451 pmcid: 8106578
Haitjema, S. et al. Loss of Y chromosome in blood is associated with major cardiovascular events during follow-up in men after carotid endarterectomy. Circ. Cardiovasc. Genet. 10, e001544. https://doi.org/10.1161/CIRCGENETICS.116.001544 (2017).
doi: 10.1161/CIRCGENETICS.116.001544 pubmed: 28768751
Vermeulen, M. C., Pearse, R., Young-Pearse, T. & Mostafavi, S. Mosaic loss of chromosome Y in aged human microglia. Genome Res. 32, 1795–1807. https://doi.org/10.1101/gr.276409.121 (2022).
doi: 10.1101/gr.276409.121 pubmed: 36041859 pmcid: 9712627
Danielsson, M. et al. Longitudinal changes in the frequency of mosaic chromosome Y loss in peripheral blood cells of aging men varies profoundly between individuals. Eur. J. Hum. Genet. 28, 349–357. https://doi.org/10.1038/s41431-019-0533-z (2020).
doi: 10.1038/s41431-019-0533-z pubmed: 31654039
Bruhn-Olszewska, B. et al. Loss of Y in leukocytes as a risk factor for critical COVID-19 in men. Genome Med. 14, 139. https://doi.org/10.1186/s13073-022-01144-5 (2022).
doi: 10.1186/s13073-022-01144-5 pubmed: 36514076 pmcid: 9747543
Ljungstrom, V. et al. Loss of Y and clonal hematopoiesis in blood-two sides of the same coin?. Leukemia 36, 889–891. https://doi.org/10.1038/s41375-021-01456-2 (2022).
doi: 10.1038/s41375-021-01456-2 pubmed: 34725452
Mattisson, J. et al. Leukocytes with chromosome Y loss have reduced abundance of the cell surface immunoprotein CD99. Sci. Rep. 11, 15160. https://doi.org/10.1038/s41598-021-94588-5 (2021).
doi: 10.1038/s41598-021-94588-5 pubmed: 34312421 pmcid: 8313698
Jakalski, M. et al. Loss of Y is associated with multi-omic changes in immune cells from Alzheimer’s disease patients. medRxiv https://doi.org/10.1101/2023.02.07.23285520 (2023).
doi: 10.1101/2023.02.07.23285520
Dumanski, J. P. et al. Mosaic loss of chromosome Y in blood is associated with Alzheimer disease. Am. J. Hum. Genet. 98, 1208–1219. https://doi.org/10.1016/j.ajhg.2016.05.014 (2016).
doi: 10.1016/j.ajhg.2016.05.014 pubmed: 27231129 pmcid: 4908225
Dumanski, J. P. et al. Smoking is associated with mosaic loss of chromosome Y. Science 347, 81–83. https://doi.org/10.1126/science.1262092 (2015).
doi: 10.1126/science.1262092 pubmed: 25477213
Sano, S. et al. Hematopoietic loss of Y chromosome leads to cardiac fibrosis and heart failure mortality. Science 377, 292–297. https://doi.org/10.1126/science.abn3100 (2022).
doi: 10.1126/science.abn3100 pubmed: 35857592 pmcid: 9437978
Binnewies, M. et al. Understanding the tumor immune microenvironment (TIME) for effective therapy. Nat. Med. 24, 541–550. https://doi.org/10.1038/s41591-018-0014-x (2018).
doi: 10.1038/s41591-018-0014-x pubmed: 29686425 pmcid: 5998822
Loddenkemper, C. et al. In situ analysis of FOXP3+ regulatory T cells in human colorectal cancer. J. Transl. Med. 4, 52. https://doi.org/10.1186/1479-5876-4-52 (2006).
doi: 10.1186/1479-5876-4-52 pubmed: 17166272 pmcid: 1764431
Toor, S. M. et al. Immune checkpoints in circulating and tumor-infiltrating CD4+ T cell subsets in colorectal cancer patients. Front. Immunol. https://doi.org/10.3389/fimmu.2019.02936 (2019).
doi: 10.3389/fimmu.2019.02936 pubmed: 31921188 pmcid: 6928042
Syed Khaja, A. S., Toor, S. M., El Salhat, H., Ali, B. R. & Elkord, E. Intratumoral FoxP3+helios+ regulatory T cells upregulating immunosuppressive molecules are expanded in human colorectal cancer. Front. Immunol. https://doi.org/10.3389/fimmu.2017.00619 (2017).
doi: 10.3389/fimmu.2017.00619 pubmed: 28603527 pmcid: 5445103
Li, C., Jiang, P., Wei, S., Xu, X. & Wang, J. Regulatory T cells in tumor microenvironment: New mechanisms, potential therapeutic strategies and future prospects. Mol. Cancer 19, 116. https://doi.org/10.1186/s12943-020-01234-1 (2020).
doi: 10.1186/s12943-020-01234-1 pubmed: 32680511 pmcid: 7367382
Frey, D. M. et al. High frequency of tumor-infiltrating FOXP3+ regulatory T cells predicts improved survival in mismatch repair-proficient colorectal cancer patients. Int. J. Cancer 126, 2635–2643. https://doi.org/10.1002/ijc.24989 (2010).
doi: 10.1002/ijc.24989 pubmed: 19856313
Ladoire, S., Martin, F. & Ghiringhelli, F. Prognostic role of FOXP3+ regulatory T cells infiltrating human carcinomas: The paradox of colorectal cancer. Cancer Immunol. Immunother. 60, 909–918. https://doi.org/10.1007/s00262-011-1046-y (2011).
doi: 10.1007/s00262-011-1046-y pubmed: 21644034
Saito, T. et al. Two FOXP3+CD4+ T cell subpopulations distinctly control the prognosis of colorectal cancers. Nat. Med. 22, 679–684. https://doi.org/10.1038/nm.4086 (2016).
doi: 10.1038/nm.4086 pubmed: 27111280
Togashi, Y., Shitara, K. & Nishikawa, H. Regulatory T cells in cancer immunosuppression—Implications for anticancer therapy. Nat. Rev. Clin. Oncol. 16, 356–371. https://doi.org/10.1038/s41571-019-0175-7 (2019).
doi: 10.1038/s41571-019-0175-7 pubmed: 30705439
Makaremi, S. et al. Immune checkpoint inhibitors in colorectal cancer: Challenges and future prospects. Biomedicines 9, 1075 (2021).
doi: 10.3390/biomedicines9091075 pubmed: 34572263 pmcid: 8467932
Keenan, T. E., Burke, K. P. & Van Allen, E. M. Genomic correlates of response to immune checkpoint blockade. Nat. Med. 25, 389–402. https://doi.org/10.1038/s41591-019-0382-x (2019).
doi: 10.1038/s41591-019-0382-x pubmed: 30842677 pmcid: 6599710
Kumagai, S. et al. The PD-1 expression balance between effector and regulatory T cells predicts the clinical efficacy of PD-1 blockade therapies. Nat. Immunol. 21, 1346–1358. https://doi.org/10.1038/s41590-020-0769-3 (2020).
doi: 10.1038/s41590-020-0769-3 pubmed: 32868929
Zhang, L. et al. Single-cell analyses inform mechanisms of myeloid-targeted therapies in colon cancer. Cell 181, 442-459.e429. https://doi.org/10.1016/j.cell.2020.03.048 (2020).
doi: 10.1016/j.cell.2020.03.048 pubmed: 32302573
Nieto, P. et al. A single-cell tumor immune atlas for precision oncology. Genome Res. 31, 1913–1926. https://doi.org/10.1101/gr.273300.120 (2021).
doi: 10.1101/gr.273300.120 pubmed: 34548323 pmcid: 8494216
Koczkowska, M. et al. Personalized health risk assessment based on single cell RNA sequencing analysis of a male with 45, X/48, XYYY karyotype. Sci. Rep. 12, 20854. https://doi.org/10.1038/s41598-022-25308-w (2022).
doi: 10.1038/s41598-022-25308-w pubmed: 36460769 pmcid: 9718746
Aristin Revilla, S., Kranenburg, O. & Coffer, P. J. Colorectal cancer-infiltrating regulatory T Cells: Functional heterogeneity, metabolic adaptation, and therapeutic targeting. Front. Immunol. 13, 903564. https://doi.org/10.3389/fimmu.2022.903564 (2022).
doi: 10.3389/fimmu.2022.903564 pubmed: 35874729 pmcid: 9304750
Mattisson, J. et al. Loss of chromosome Y in regulatory T cells. BMC Genom. https://doi.org/10.1186/s12864-024-10168-7 (2024).
doi: 10.1186/s12864-024-10168-7
Saleh, R. & Elkord, E. FoxP3+ T regulatory cells in cancer: Prognostic biomarkers and therapeutic targets. Cancer Lett. 490, 174–185. https://doi.org/10.1016/j.canlet.2020.07.022 (2020).
doi: 10.1016/j.canlet.2020.07.022 pubmed: 32721551
Ahmadzadeh, M. et al. FOXP3 expression accurately defines the population of intratumoral regulatory T cells that selectively accumulate in metastatic melanoma lesions. Blood 112, 4953–4960. https://doi.org/10.1182/blood-2008-06-163048 (2008).
doi: 10.1182/blood-2008-06-163048 pubmed: 18820132 pmcid: 2954707
Kotsakis, A. et al. Prognostic value of circulating regulatory T cell subsets in untreated non-small cell lung cancer patients. Sci. Rep. https://doi.org/10.1038/srep39247 (2016).
doi: 10.1038/srep39247 pubmed: 27976733 pmcid: 5157012
Kim, J. H., Kim, B. S. & Lee, S. K. Regulatory T cells in tumor microenvironment and approach for anticancer immunotherapy. Immune Netw. 20, e4. https://doi.org/10.4110/in.2020.20.e4 (2020).
doi: 10.4110/in.2020.20.e4 pubmed: 32158592 pmcid: 7049587
Sasidharan Nair, V. & Elkord, E. Immune checkpoint inhibitors in cancer therapy: A focus on T-regulatory cells. Immunol. Cell Biol. 96, 21–33. https://doi.org/10.1111/imcb.1003 (2018).
doi: 10.1111/imcb.1003 pubmed: 29359507
Chaudhary, B. & Elkord, E. Regulatory T cells in the tumor microenvironment and cancer progression: Role and therapeutic targeting. Vaccines 4, 28. https://doi.org/10.3390/vaccines4030028 (2016).
doi: 10.3390/vaccines4030028 pubmed: 27509527 pmcid: 5041022
Shang, B., Liu, Y., Jiang, S. J. & Liu, Y. Prognostic value of tumor-infiltrating FoxP3+ regulatory T cells in cancers: A systematic review and meta-analysis. Sci. Rep. https://doi.org/10.1038/srep15179 (2015).
doi: 10.1038/srep15179 pubmed: 26686764 pmcid: 4685263
Ward-Hartstonge, K. A. & Kemp, R. A. Regulatory T-cell heterogeneity and the cancer immune response. Clin. Transl. Immunol. 6, e154. https://doi.org/10.1038/cti.2017.43 (2017).
doi: 10.1038/cti.2017.43
Wang, S. et al. Interleukin-10 deficiency impairs regulatory T cell-derived neuropilin-1 functions and promotes Th1 and Th17 immunity. Sci. Rep. 6, 24249 (2016).
doi: 10.1038/srep24249 pubmed: 27075020 pmcid: 4831052
Abdel-Hafiz, H. A. et al. Y chromosome loss in cancer drives growth by evasion of adaptive immunity. Nature 619, 624–631. https://doi.org/10.1038/s41586-023-06234-x (2023).
doi: 10.1038/s41586-023-06234-x pubmed: 37344596 pmcid: 10975863
Duijf, P. H., Schultz, N. & Benezra, R. Cancer cells preferentially lose small chromosomes. Int. J. Cancer 132, 2316–2326. https://doi.org/10.1002/ijc.27924 (2013).
doi: 10.1002/ijc.27924 pubmed: 23124507
Müller, P. et al. Why loss of Y? A pan-cancer genome analysis of tumors with loss of Y chromosome. Comput. Struct. Biotechnol. J. 21, 1573–1583. https://doi.org/10.1016/j.csbj.2023.02.024 (2023).
doi: 10.1016/j.csbj.2023.02.024 pubmed: 36874157 pmcid: 9978323
Mitchell, E. et al. Clonal dynamics of haematopoiesis across the human lifespan. Nature 606, 343–350. https://doi.org/10.1038/s41586-022-04786-y (2022).
doi: 10.1038/s41586-022-04786-y pubmed: 35650442 pmcid: 9177428
Cook, M. B., McGlynn, K. A., Devesa, S. S., Freedman, N. D. & Anderson, W. F. Sex disparities in cancer mortality and survival. Cancer Epidemiol. Biomark. Prev. 20, 1629–1637 (2011).
doi: 10.1158/1055-9965.EPI-11-0246
Edgren, G., Liang, L., Adami, H. O. & Chang, E. T. Enigmatic sex disparities in cancer incidence. Eur. J. Epidemiol. 27, 187–196 (2012).
doi: 10.1007/s10654-011-9647-5 pubmed: 22212865
Siegel, R. L., Miller, K. D., Fuchs, H. E. & Jemal, A. Cancer statistics, 2022. CA Cancer J. Clin. 72, 7–33. https://doi.org/10.3322/caac.21708 (2022).
doi: 10.3322/caac.21708 pubmed: 35020204
Pohl, S. T., Prada, M. L., Espinet, E. & Jurkowska, R. Practical considerations for complex tissue dissociation for single-cell transcriptomics. Methods Mol. Biol. 2584, 371–387. https://doi.org/10.1007/978-1-0716-2756-3_19 (2023).
doi: 10.1007/978-1-0716-2756-3_19 pubmed: 36495461
Filipowicz, N. et al. Comprehensive cancer-oriented biobanking resource of human samples for studies of post-zygotic genetic variation involved in cancer predisposition. PLoS One 17, e0266111. https://doi.org/10.1101/2021.09.03.458865 (2022).
doi: 10.1101/2021.09.03.458865 pubmed: 35390022 pmcid: 8989288
Hao, Y. et al. Integrated analysis of multimodal single-cell data. Cell 184, 3573-3587e3529. https://doi.org/10.1016/j.cell.2021.04.048 (2021).
doi: 10.1016/j.cell.2021.04.048 pubmed: 34062119 pmcid: 8238499

Auteurs

Magdalena Wójcik (M)

3P-Medicine Laboratory, Medical University of Gdańsk, Dębinki 7, 80-211, Gdańsk, Poland.

Ulana Juhas (U)

3P-Medicine Laboratory, Medical University of Gdańsk, Dębinki 7, 80-211, Gdańsk, Poland.
Department of Bioenergetics and Physiology of Exercise, Medical University of Gdańsk, Dębinki 1, 80-211, Gdańsk, Poland.

Elyas Mohammadi (E)

3P-Medicine Laboratory, Medical University of Gdańsk, Dębinki 7, 80-211, Gdańsk, Poland.

Jonas Mattisson (J)

Department of Immunology, Genetics and Pathology and Science for Life Laboratory, Uppsala University, Uppsala, Sweden.

Kinga Drężek-Chyła (K)

3P-Medicine Laboratory, Medical University of Gdańsk, Dębinki 7, 80-211, Gdańsk, Poland.

Edyta Rychlicka-Buniowska (E)

3P-Medicine Laboratory, Medical University of Gdańsk, Dębinki 7, 80-211, Gdańsk, Poland.

Bożena Bruhn-Olszewska (B)

Department of Immunology, Genetics and Pathology and Science for Life Laboratory, Uppsala University, Uppsala, Sweden.

Hanna Davies (H)

Department of Immunology, Genetics and Pathology and Science for Life Laboratory, Uppsala University, Uppsala, Sweden.

Katarzyna Chojnowska (K)

3P-Medicine Laboratory, Medical University of Gdańsk, Dębinki 7, 80-211, Gdańsk, Poland.

Paweł Olszewski (P)

3P-Medicine Laboratory, Medical University of Gdańsk, Dębinki 7, 80-211, Gdańsk, Poland.

Michał Bieńkowski (M)

Department of Pathomorphology, Medical University of Gdańsk, Gdańsk, Poland.

Michał Jankowski (M)

Surgical Oncology, Ludwik Rydygier's Collegium Medicum, Bydgoszcz, Nicolaus Copernicus University, Toruń, Poland.
Department of Surgical Oncology, Oncology Center - Prof. Franciszek Łukaszczyk Memorial Hospital, Bydgoszcz, Poland.

Olga Rostkowska (O)

Department of Oncological, Transplant and General Surgery, Medical University of Gdańsk, Gdańsk, Poland.

Andrzej Hellmann (A)

Department of Oncological, Transplant and General Surgery, Medical University of Gdańsk, Gdańsk, Poland.

Rafał Pęksa (R)

Department of Pathomorphology, Medical University of Gdańsk, Gdańsk, Poland.

Jacek Kowalski (J)

Department of Pathomorphology, Medical University of Gdańsk, Gdańsk, Poland.

Marek Zdrenka (M)

Department of Tumor Pathology and Pathomorphology, Oncology Center - Prof. Franciszek Łukaszczyk Memorial Hospital, Bydgoszcz, Poland.

Jarek Kobiela (J)

Department of Oncological, Transplant and General Surgery, Medical University of Gdańsk, Gdańsk, Poland.

Wojciech Zegarski (W)

Surgical Oncology, Ludwik Rydygier's Collegium Medicum, Bydgoszcz, Nicolaus Copernicus University, Toruń, Poland.
Department of Surgical Oncology, Oncology Center - Prof. Franciszek Łukaszczyk Memorial Hospital, Bydgoszcz, Poland.

Wojciech Biernat (W)

Department of Pathomorphology, Medical University of Gdańsk, Gdańsk, Poland.

Łukasz Szylberg (Ł)

Department of Tumor Pathology and Pathomorphology, Oncology Center - Prof. Franciszek Łukaszczyk Memorial Hospital, Bydgoszcz, Poland.
Department of Clinical Pathomorphology, Collegium Medicum in Bydgoszcz, Nicolaus Copernicus University in Toruń, Bydgoszcz, Poland.

Piotr Remiszewski (P)

Department of Oncological, Transplant and General Surgery, Medical University of Gdańsk, Gdańsk, Poland.

Jakub Mieczkowski (J)

3P-Medicine Laboratory, Medical University of Gdańsk, Dębinki 7, 80-211, Gdańsk, Poland.

Natalia Filipowicz (N)

3P-Medicine Laboratory, Medical University of Gdańsk, Dębinki 7, 80-211, Gdańsk, Poland. natalia.filipowicz@gumed.edu.pl.

Jan P Dumanski (JP)

3P-Medicine Laboratory, Medical University of Gdańsk, Dębinki 7, 80-211, Gdańsk, Poland. jan.dumanski@igp.uu.se.
Department of Immunology, Genetics and Pathology and Science for Life Laboratory, Uppsala University, Uppsala, Sweden. jan.dumanski@igp.uu.se.

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Classifications MeSH

questionsmedicales.fr › Eucaryotes › Animaux › Chordés › Vertébrés › Mammifères › Eutheria › Primates › Haplorhini › Catarrhini › Hominidae › Humains › Loss of Y in regulatory T lymphocytes in the...
questionsmedicales.fr › Maladies de l'appareil digestif › Maladies gastro-intestinales › Maladies intestinales › Maladies du rectum › Tumeurs colorectales › Loss of Y in regulatory T lymphocytes in the...
questionsmedicales.fr › Phénomènes physiologiques cellulaires › Microenvironnement cellulaire › Microenvironnement tumoral › Loss of Y in regulatory T lymphocytes in the...
questionsmedicales.fr › Systèmes sanguin et immunitaire › Système immunitaire › Leucocytes › Agranulocytes › Lymphocytes › Lymphocytes T › Sous-populations de lymphocytes T › Lymphocytes T régulateurs › Loss of Y in regulatory T lymphocytes in the...
questionsmedicales.fr › Maladies de l'appareil digestif › Maladies du foie › Tumeurs du foie › Loss of Y in regulatory T lymphocytes in the...
questionsmedicales.fr › Personnes › Tranches d'âge › Adulte › Sujet âgé › Loss of Y in regulatory T lymphocytes in the...
questionsmedicales.fr › Facteurs biologiques › Marqueurs biologiques › Antigènes de différenciation › Antigènes de différenciation des lymphocytes T › Récepteur-1 de mort cellulaire programmée › Loss of Y in regulatory T lymphocytes in the...
questionsmedicales.fr › Personnes › Tranches d'âge › Adulte › Adulte d'âge moyen › Loss of Y in regulatory T lymphocytes in the...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Protéines membranaires › Récepteurs de surface cellulaire › Récepteurs immunologiques › Loss of Y in regulatory T lymphocytes in the...
questionsmedicales.fr › Systèmes sanguin et immunitaire › Système immunitaire › Leucocytes › Agranulocytes › Lymphocytes › Lymphocytes TIL › Loss of Y in regulatory T lymphocytes in the...
questionsmedicales.fr › Acides aminés, peptides et protéines › Protéines › Facteurs de transcription › Facteurs de transcription Krüppel-like › Facteur de transcription Ikaros › Loss of Y in regulatory T lymphocytes in the...