Prognostic value of tumour-associated regulatory T-cells as a biomarker in non-small cell lung cancer: a systematic review and meta-analysis.


Journal

Systematic reviews
ISSN: 2046-4053
Titre abrégé: Syst Rev
Pays: England
ID NLM: 101580575

Informations de publication

Date de publication:
14 Sep 2024
Historique:
received: 11 02 2024
accepted: 20 08 2024
medline: 14 9 2024
pubmed: 14 9 2024
entrez: 13 9 2024
Statut: epublish

Résumé

Tumour, nodes, and metastases (TNM) staging has been deficient in prognosticating in patients suffering from non-small cell lung cancer (NSCLC). To supplement TNM staging, this systematic review and meta-analysis aimed to evaluate the prognostic value of the regulatory T cells (Treg). A keyword search was conducted in MEDLINE and EMBASE for full-text original human studies from any region published in English during the last 12 years. Eligible for inclusion were studies evaluating the prognostic value of the number of Treg cells in NSCLC except case studies, case series, systematic reviews, and meta-analyses. Two reviewers (one reviewer used an automation tool) independently screened the studies and assessed risk-of-bias using the Quality in Prognosis Studies (QUIPS) tool. Meta-analysis was done for studies reporting significant multivariate hazard ratio (HR). Out of 809 retrievals, 24 studies were included in the final review. The low number of Treg cells was found significantly associated with improved overall survival (pooled log OR, 1.646; 95% CI, 1.349, 1.944; p (2-tailed) < .001; SE, 0.1217), improved recurrence-free survival (HR, 1.99; 95% CI, 1.15, 3.46; p = .01), improved progression-free survival (pooled log OR, 2.231; 95% CI, 0.424, 4.038; p (2-tailed) .034; SE, 0.4200), and worse disease-free survival (pooled log OR, 0.992; 95% CI, 0.820, 1.163; p (2-tailed) .009; SE, 0.0135), especially when identified by forkhead box P3 (FOXP3), in any stage or non-metastatic NSCLC. A low number of Treg cells indicated better survival, suggesting its potential use as a prognostic biomarker in NSCLC. The protocol of this review was prospectively registered on PROSPERO on August 28, 2021, and was assigned the registration number CRD42021270598. The protocol can be accessed from PROSPERO website.

Sections du résumé

BACKGROUND BACKGROUND
Tumour, nodes, and metastases (TNM) staging has been deficient in prognosticating in patients suffering from non-small cell lung cancer (NSCLC). To supplement TNM staging, this systematic review and meta-analysis aimed to evaluate the prognostic value of the regulatory T cells (Treg).
METHODS METHODS
A keyword search was conducted in MEDLINE and EMBASE for full-text original human studies from any region published in English during the last 12 years. Eligible for inclusion were studies evaluating the prognostic value of the number of Treg cells in NSCLC except case studies, case series, systematic reviews, and meta-analyses. Two reviewers (one reviewer used an automation tool) independently screened the studies and assessed risk-of-bias using the Quality in Prognosis Studies (QUIPS) tool. Meta-analysis was done for studies reporting significant multivariate hazard ratio (HR).
RESULTS RESULTS
Out of 809 retrievals, 24 studies were included in the final review. The low number of Treg cells was found significantly associated with improved overall survival (pooled log OR, 1.646; 95% CI, 1.349, 1.944; p (2-tailed) < .001; SE, 0.1217), improved recurrence-free survival (HR, 1.99; 95% CI, 1.15, 3.46; p = .01), improved progression-free survival (pooled log OR, 2.231; 95% CI, 0.424, 4.038; p (2-tailed) .034; SE, 0.4200), and worse disease-free survival (pooled log OR, 0.992; 95% CI, 0.820, 1.163; p (2-tailed) .009; SE, 0.0135), especially when identified by forkhead box P3 (FOXP3), in any stage or non-metastatic NSCLC.
CONCLUSION CONCLUSIONS
A low number of Treg cells indicated better survival, suggesting its potential use as a prognostic biomarker in NSCLC.
SYSTEMATIC REVIEW REGISTRATION BACKGROUND
The protocol of this review was prospectively registered on PROSPERO on August 28, 2021, and was assigned the registration number CRD42021270598. The protocol can be accessed from PROSPERO website.

Identifiants

pubmed: 39272135
doi: 10.1186/s13643-024-02642-w
pii: 10.1186/s13643-024-02642-w
doi:

Substances chimiques

Biomarkers, Tumor 0

Types de publication

Journal Article Systematic Review Meta-Analysis

Langues

eng

Sous-ensembles de citation

IM

Pagination

233

Informations de copyright

© 2024. The Author(s).

Références

American Cancer Society. Lung Cancer. In: The Cancer Atlas. 2019.
Zappa C, Mousa S. Non-small cell lung cancer: current treatment and future advances. Transl Lung Cancer Res. 2016;5(3):288.
pubmed: 27413711 pmcid: 4931124 doi: 10.21037/tlcr.2016.06.07
National Cancer Institute. Surveillance, epidemiology, and end results program. 2023. Available from: https://seer.cancer.gov/ . [Cited 2023 Aug 20].
Howlader N, Forjaz G, Mooradian MJ, Meza R, Kong CY, Cronin KA, et al. The effect of advances in lung-cancer treatment on population mortality. N Engl J Med. 2020Aug 13;383(7):640–9.
pubmed: 32786189 pmcid: 8577315 doi: 10.1056/NEJMoa1916623
Goldstraw P, Ball D, Jett J, Le Chevalier T, Lim E, Nicholson A, et al. Non-small-cell lung cancer. Lancet (London, England). 2011;378(9804):1727–40.
pubmed: 21565398 doi: 10.1016/S0140-6736(10)62101-0
Kameyama K, Huang CL, Liu D, Okamoto T, Hayashi E, Yamamoto Y, et al. Problems related to TNM staging: patients with stage III non–small cell lung cancer. J Thorac Cardiovasc Surg. 2002;124(3):503–10.
pubmed: 12202867 doi: 10.1067/mtc.2002.123810
IASLC. International association for the study of lung cancer. 2023. Available from: https://www.iaslc.org/ . [Cited 2023 Aug 20].
Rami-Porta R, Goldstraw P. Strength and weakness of the new TNM classification for lung cancer. Eur Respir J. 2010;36(2):237–9.
pubmed: 20675779 doi: 10.1183/09031936.00016210
Hattori A, Takamochi K, Oh S, Suzuki K. New revisions and current issues in the eighth edition of the TNM classification for non-small cell lung cancer. Jpn J Clin Oncol. 2019;49(1):3–11.
pubmed: 30277521 doi: 10.1093/jjco/hyy142
Bates G, Fox S, Han C, Leek R, Garcia J, Harris A, et al. Quantification of regulatory T cells enables the identification of high-risk breast cancer patients and those at risk of late relapse. J Clin Oncol. 2006;24(34):5373–80.
pubmed: 17135638 doi: 10.1200/JCO.2006.05.9584
Clemente C, Mihm M, Bufalino R, Zurrida S, Collini P, Cascinelli N. Prognostic value of tumor infiltrating lymphocytes in the vertical growth phase of primary cutaneous melanoma. Cancer. 1996;77(7):1303–10.
pubmed: 8608507 doi: 10.1002/(SICI)1097-0142(19960401)77:7<1303::AID-CNCR12>3.0.CO;2-5
Galon J, Costes A, Sanchez-Cabo F, Kirilovsky A, Mlecnik B, Lagorce-Pagès C, et al. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome. Science (New York, NY). 2006;313(5795):1960–4.
doi: 10.1126/science.1129139
Johnson S, Kerr K, Chapman A, Kennedy M, King G, Cockburn J, et al. Immune cell infiltrates and prognosis in primary carcinoma of the lung. Lung cancer (Amsterdam, Netherlands). 2000;27(1):27–35.
pubmed: 10672781 doi: 10.1016/S0169-5002(99)00095-1
Marrogi A, Munshi A, Merogi A, Ohadike Y, El-Habashi A, Marrogi O, et al. Study of tumor infiltrating lymphocytes and transforming growth factor-beta as prognostic factors in breast carcinoma. Int J Cancer. 1997;74(5):492–501.
pubmed: 9355970 doi: 10.1002/(SICI)1097-0215(19971021)74:5<492::AID-IJC3>3.0.CO;2-Z
Ropponen KM, Eskelinen MJ, Lipponen PK, Alhava EKVM. Prognostic value of tumour-infiltrating lymphocytes (TILs) in colorectal cancer-PubMed. J Pathol. 1997;182(3):318–24.
pubmed: 9349235 doi: 10.1002/(SICI)1096-9896(199707)182:3<318::AID-PATH862>3.0.CO;2-6
Vesalainen S, Lipponen P, Talja M, Syrjänen K. Histological grade, perineural infiltration, tumour-infiltrating lymphocytes and apoptosis as determinants of long-term prognosis in prostatic adenocarcinoma.  Eur J Cancer (Oxford, England: 1990). 1994;30A(12):1797–803.
Al-Shibli K, Donnem TS, AlSaad S, Persson M, Bremnes R, Busund L. Prognostic effect of epithelial and stromal lymphocyte infiltration in non-small cell lung cancer. Clin Cancer Res. 2008;14(16):5220–7.
pubmed: 18698040 doi: 10.1158/1078-0432.CCR-08-0133
Fridman W, Pagès F, Sautès-Fridman C, Galon J. The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer. 2012;12(4):298–306.
pubmed: 22419253 doi: 10.1038/nrc3245
Donnem T, Kilvaer T, Andersen S, Richardsen E, Paulsen E, Hald S, et al. Strategies for clinical implementation of TNM-Immunoscore in resected nonsmall-cell lung cancer. Ann Oncol. 2016;27(2):225–32.
pubmed: 26578726 doi: 10.1093/annonc/mdv560
Mlecnik B, Tosolini M, Kirilovsky A, Berger A, Bindea G, Meatchi T, et al. Histopathologic-based prognostic factors of colorectal cancers are associated with the state of the local immune reaction. J Clin Oncol. 2011;29(6):610–8.
pubmed: 21245428 doi: 10.1200/JCO.2010.30.5425
Yang Y, Yang X, Wang Y, Xu J, Shen H, Gou H, et al. Combined consideration of tumor-associated immune cell density and immune checkpoint expression in the peritumoral microenvironment for prognostic stratification of non-small-cell lung cancer patients. Front Immunol. 2022;10:13.
Parra ER, Behrens C, Rodriguez-Canales J, Lin H, Mino B, Blando J, et al. Image analysis-based assessment of PD-L1 and tumor-associated immune cells density supports distinct intratumoral microenvironment groups in non-small cell lung carcinoma patients. Clin Cancer Res. 2016;22(24):6278–89.
pubmed: 27252415 pmcid: 5558040 doi: 10.1158/1078-0432.CCR-15-2443
Fridman W, Pagès F, Sautès-Fridman C, Galon J. The immune contexture in human tumours: impact on clinical outcome. Nat Rev Cancer. 2012;12(4):298–306.
pubmed: 22419253 doi: 10.1038/nrc3245
Ganesan A, Johansson M, Ruffell B, Yagui-Beltrán A, Lau J, Jablons D, et al. Tumor-infiltrating regulatory T cells inhibit endogenous cytotoxic T cell responses to lung adenocarcinoma. J Immunol. 2013;191(4):2009–17.
pubmed: 23851682 doi: 10.4049/jimmunol.1301317
Platonova S, Cherfils-Vicini J, Damotte D, Crozet L, Vieillard V, Validire P, et al. Profound coordinated alterations of intratumoral NK cell phenotype and function in lung carcinoma. Can Res. 2011;71(16):5412–22.
doi: 10.1158/0008-5472.CAN-10-4179
Kim R, Emi M, Tanabe K. Cancer immunoediting from immune surveillance to immune escape. Immunology. 2007;121(1):1.
pubmed: 17386080 pmcid: 2265921 doi: 10.1111/j.1365-2567.2007.02587.x
Schreiber R, Old L, Smyth M. Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion. Science (New York, NY). 2011;331(6024):1565–70.
doi: 10.1126/science.1203486
Mittal D, Gubin M, Schreiber R, Smyth M. New insights into cancer immunoediting and its three component phases–elimination, equilibrium and escape. Curr Opin Immunol. 2014;27(1):16–25.
pubmed: 24531241 pmcid: 4388310 doi: 10.1016/j.coi.2014.01.004
Dunn G, Old L, Schreiber R. The immunobiology of cancer immunosurveillance and immunoediting. Immunity. 2004;21(2):137–48.
pubmed: 15308095 doi: 10.1016/j.immuni.2004.07.017
Schreiber R, Old L, Smyth M. Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion. Science (New York, NY). 2011;331(6024):1565–70.
doi: 10.1126/science.1203486
Mittal D, Gubin M, Schreiber R, Smyth M. New insights into cancer immunoediting and its three component phases–elimination, equilibrium and escape. Curr Opin Immunol. 2014;27(1):16–25.
pubmed: 24531241 pmcid: 4388310 doi: 10.1016/j.coi.2014.01.004
Dunn G, Old L, Schreiber R. The immunobiology of cancer immunosurveillance and immunoediting. Immunity. 2004;21(2):137–48.
pubmed: 15308095 doi: 10.1016/j.immuni.2004.07.017
Takeuchi Y, Nishikawa H. Roles of regulatory T cells in cancer immunity. Int Immunol. 2016;28(8):401–9.
pubmed: 27160722 pmcid: 4986235 doi: 10.1093/intimm/dxw025
Fantini MC, Favale A, Onali S, Facciotti F. Tumor infiltrating regulatory T cells in sporadic and colitis-associated colorectal cancer: the red little riding hood and the wolf. Int J Mol Sci. 2020;21(18):6744.
pubmed: 32937953 pmcid: 7555219 doi: 10.3390/ijms21186744
Cinier J, Hubert M, Besson L, Di Roio A, Rodriguez C, Lombardi V, et al. Recruitment and expansion of Tregs cells in the tumor environment-how to target them? Cancers. 2021;13(8):1850.
Kotsakis A, Koinis F, Katsarou A, Gioulbasani M, Aggouraki D, Kentepozidis N, et al. Prognostic value of circulating regulatory T cell subsets in untreated non-small cell lung cancer patients. Sci Rep. 2016;6(1):1–11.
doi: 10.1038/srep39247
Erfani N, Mehrabadi SM, Ghayumi MA, Haghshenas MR, Mojtahedi Z, Ghaderi A, et al. Increase of regulatory T cells in metastatic stage and CTLA-4 over expression in lymphocytes of patients with non-small cell lung cancer (NSCLC). Lung Cancer. 2012A 1;77(2):306–11.
pubmed: 22608141 doi: 10.1016/j.lungcan.2012.04.011
Basumallik N, Agarwal M. Small Cell Lung Cancer. [Updated 2023 Jul 10]. In: StatPearls [Internet]. Treasure Island: StatPearls Publishing; 2024. Available from: https://www.ncbi.nlm.nih.gov/books/NBK482458/ .
Higgins J, Lasserson T, Thomas J, Flemyng E, Churchill R. Cochrane Community. 2023. Methodological expectations of cochrane intervention reviews: standards for the conduct of new Cochrane intervention reviews, and the planning and conduct of updates. Available from: https://community.cochrane.org/mecir-manual . [Cited 2024 Aug 3].
Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ. 2021;29:372.
Yang S, Liu Y, Li MY, Ng CSH, Yang S li, Wang S, et al. FOXP3 promotes tumor growth and metastasis by activating Wnt/β-catenin signaling pathway and EMT in non-small cell lung cancer. Mol Cancer. 2017;16(1):124.
Peng H, Wu X, Zhong R, Yu T, Cai X, Liu J, et al. Profiling tumor immune microenvironment of non-small cell lung cancer using multiplex immunofluorescence. Front Immunol. 2021;4:12.
Germain C, Devi-Marulkar P, Knockaert S, Biton J, Kaplon H, Letaïef L, et al. Tertiary lymphoid structure-B cells narrow regulatory t cells impact in lung cancer patients. Front Immunol. 2021;8:12.
Riemann D, Cwikowski M, Turzer S, Giese T, Grallert M, Schütte W, et al. Blood immune cell biomarkers in lung cancer. Clin Exp Immunol. 2019F 1;195(2):179–89.
pubmed: 30246868 doi: 10.1111/cei.13219
Ameratunga M, Asadi K, Lin X, Walkiewicz M, Murone C, Knight S, et al. PD-L1 and tumor infiltrating lymphocytes as prognostic markers in resected NSCLC. PLoS One. 2016;11(4):e0153954.
Parra ER, Jiang M, Machado-Rugolo J, Yaegashi LB, Prieto T, Farhat C, et al. Variants in epithelial-mesenchymal transition and immune checkpoint genes are associated with immune cell profiles and predict survival in non-small cell lung cancer. Arch Pathol Lab Med. 2020;144(10):1234–44.
pubmed: 32150457 doi: 10.5858/arpa.2019-0419-OA
Liu C, Wu S, Meng X, Liu G, Chen D, Cong Y, et al. Predictive value of peripheral regulatory T cells in non-small cell lung cancer patients undergoing radiotherapy. Oncotarget. 2017;8(26):43427–38.
pubmed: 28624781 pmcid: 5522158 doi: 10.18632/oncotarget.15238
Barua S, Fang P, Sharma A, Fujimoto J, Wistuba I, Rao AUK, et al. Spatial interaction of tumor cells and regulatory T cells correlates with survival in non-small cell lung cancer. Lung Cancer. 2018;1(117):73–9.
doi: 10.1016/j.lungcan.2018.01.022
Yaegashi LB, Baldavira CM, Prieto TG, Machado-Rugolo J, Velosa APP, da Silveira LKR, et al. In situ overexpression of matricellular mechanical proteins demands functional immune signature and mitigates non-small cell lung cancer progression. Front Immunol. 2021A;16:12.
Yan X, Jiao SC, Zhang GQ, Guan Y, Wang JL. Tumor-associated immune factors are associated with recurrence and metastasis in non-small cell lung cancer. Cancer Gene Ther. 2017;24(2):57–63.
pubmed: 28084319 pmcid: 5339429 doi: 10.1038/cgt.2016.40
Kotsakis A, Koinis F, Katsarou A, Gioulbasani M, Aggouraki D, Kentepozidis N, et al. Prognostic value of circulating regulatory T cell subsets in untreated non-small cell lung cancer patients. Sci Rep. 2016;15:6.
Kinoshita T, Muramatsu R, Fujita T, Nagumo H, Sakurai T, Noji S, et al. Prognostic value of tumor-infiltrating lymphocytes differs depending on histological type and smoking habit in completely resected non-small-cell lung cancer. Ann Oncol. 2016;27(11):2117–23.
pubmed: 27502728 doi: 10.1093/annonc/mdw319
Aldarouish M, Su X, Qiao J, Gao C, Chen Y, Dai A, et al. Immunomodulatory effects of chemotherapy on blood lymphocytes and survival of patients with advanced non-small cell lung cancer. Int J Immunopathol Pharmacol. 2019;33:1-9.
Muto S, Owada Y, Inoue T, Watanabe Y, Yamaura T, Fukuhara M, et al. Clinical significance of expanded Foxp3
pubmed: 26460798 pmcid: 4665856 doi: 10.3892/ijo.2015.3196
Hao J, Wang H, Song L, Li S, Che N, Zhang S, et al. Infiltration of CD8+ FOXP3+ T cells, CD8+ T cells, and FOXP3+ T cells in non-small cell lung cancer microenvironment. Int J Clin Exp Pathol. 2020;13(5):880.
pubmed: 32509058 pmcid: 7270696
Schulze AB, Evers G, Görlich D, Mohr M, Marra A, Hillejan L, et al. Tumor infiltrating T cells influence prognosis in stage I-III non-small cell lung cancer. J Thorac Dis. 2020;12(5):1824–42.
pubmed: 32642087 pmcid: 7330340 doi: 10.21037/jtd-19-3414a
Hasegawa T, Suzuki H, Yamaura T, Muto S, Okabe N, Osugi J, et al. Prognostic value of peripheral and local forkhead box P3+ regulatory T cells in patients with non-small-cell lung cancer. Mol Clin Oncol. 2014;2(5):685–94.
pubmed: 25054031 pmcid: 4106667 doi: 10.3892/mco.2014.299
Teng F, Meng X, Wang X, Yuan J, Liu S, Mu D, et al. Expressions of CD8+TILs, PD-L1 and Foxp3+TILs in stage I NSCLC guiding adjuvant chemotherapy decisions. Oncotarget. 2016;7(39):64318–29.
pubmed: 27602763 pmcid: 5325445 doi: 10.18632/oncotarget.11793
Usó M, Jantus-Lewintre E, Bremnes RM, Calabuig S, Blasco A, Pastor E, et al. Analysis of the immune microenvironment in resected non-small cell lung cancer: the prognostic value of different T lymphocyte markers. Oncotarget. 2016;7(33):52849–61.
pubmed: 27463005 pmcid: 5288153 doi: 10.18632/oncotarget.10811
Gelibter A, Asquino A, Strigari L, Zizzari IG, Tuosto L, Scirocchi F, et al. CD137+ and regulatory T cells as independent prognostic factors of survival in advanced non-oncogene addicted NSCLC patients treated with immunotherapy as first-line. J Transl Med. 2024;22(1). Available from: https://pubmed.ncbi.nlm.nih.gov/38570798/ . [Cited 2024 Aug 3].
Devi-Marulkar P, Fastenackels S, Karapentiantz P, Goc J, Germain C, Kaplon H, et al. Regulatory T cells infiltrate the tumor-induced tertiary lymphoïd structures and are associated with poor clinical outcome in NSCLC. Commun Biol. 2022;5(1). Available from: https://pubmed.ncbi.nlm.nih.gov/36566320/ . [Cited 2024 Aug 3].
Liu C, Sun B, Hu X, Zhang Y, Wang Q, Yue J, et al. Stereotactic ablative radiation therapy for pulmonary recurrence-based oligometastatic non-small cell lung cancer: survival and prognostic value of regulatory T cells. Int J Radiat Oncol Biol Phys. 2019;105(5):1055–64. Available from: https://pubmed.ncbi.nlm.nih.gov/31437470/ . [Cited 2024 Aug 3].
Meng X, Gao Y, Yang L, Jing H, Teng F, Huang Z, et al. Immune microenvironment differences between squamous and non-squamous non-small-cell lung cancer and their influence on the prognosis. Clin Lung Cancer. 2019;20(1):48–58. Available from: https://pubmed.ncbi.nlm.nih.gov/30341017/ . [Cited 2024 Aug 3].
Rutkowski J, Cyman M, Ślebioda T, Bemben K, Rutkowska A, Gruchała M, et al. Evaluation of peripheral blood T lymphocyte surface activation markers and transcription factors in patients with early stage non-small cell lung cancer. Cell Immunol. 2017;322:26–33. Available from: https://pubmed.ncbi.nlm.nih.gov/28939130/ . [Cited 2024 Aug 3].
Liang J, Bi G, Shan G, Jin X, Bian Y, Wang Q. Tumor-associated regulatory T cells in non-small-cell lung cancer: current advances and future perspectives. J Immunol Res. 2022;2022:4355386.
pubmed: 35497874 pmcid: 9054468 doi: 10.1155/2022/4355386
Mahmud SA, Manlove LS, Schmitz HM, Xing Y, Wang Y, Owen DL, et al. Costimulation via the tumor-necrosis factor receptor superfamily couples TCR signal strength to the thymic differentiation of regulatory T cells. Nat Immunol. 2014;15(5):473–81.
pubmed: 24633226 pmcid: 4000541 doi: 10.1038/ni.2849
Speeckaert R, Vermaelen K, Van Geel N, Autier P, Lambert J, Haspeslagh M, et al. Indoleamine 2,3-dioxygenase, a new prognostic marker in sentinel lymph nodes of melanoma patients. Eur J Cancer. 2012;48(13):2004–11.
pubmed: 22033321 doi: 10.1016/j.ejca.2011.09.007
Principe DR, Doll JA, Bauer J, Jung B, Munshi HG, Bartholin L, et al. TGF-β: duality of function between tumor prevention and carcinogenesis. J Natl Cancer Inst. 2014;106(2):djt369.
Smith C, Chang MY, Parker KH, Beury DW, DuHadaway JB, Flick HE, et al. IDO is a nodal pathogenic driver of lung cancer and metastasis development. Cancer Discov. 2012;2(8):722–35.
pubmed: 22822050 pmcid: 3677576 doi: 10.1158/2159-8290.CD-12-0014
Wang H, Franco F, Ho PC. Metabolic regulation of Tregs in cancer: opportunities for immunotherapy. Trends in Cancer. 2017;3(8):583–92.
pubmed: 28780935 doi: 10.1016/j.trecan.2017.06.005
Angelin A, Gil-de-Gómez L, Dahiya S, Jiao J, Guo L, Levine MH, et al. Foxp3 reprograms T cell metabolism to function in low-glucose, high-lactate environments. Cell Metab. 2017;25(6):1282-1293.e7.
pubmed: 28416194 pmcid: 5462872 doi: 10.1016/j.cmet.2016.12.018
Wang S, Zhang Y, Wang Y, Ye P, Li J, Li H, et al. Amphiregulin confers regulatory T cell suppressive function and tumor invasion via the EGFR/GSK-3β/Foxp3 axis. J Biol Chem. 2016;291(40):21085–95.
pubmed: 27432879 pmcid: 5076518 doi: 10.1074/jbc.M116.717892
Zhang CY, Qi Y, Li XN, Yang Y, Liu D, Zhao J, et al. The role of CCL20/CCR6 axis in recruiting Treg cells to tumor sites of NSCLC patients. Biomed Pharmacother. 2015;69:242–8.
pubmed: 25661365 doi: 10.1016/j.biopha.2014.12.008
Zdanov S, Mandapathil M, Eid RA, Adamson-Fadeyi S, Wilson W, Qian J, et al. Mutant KRAS conversion of conventional T cells into regulatory T cells. Cancer Immunol Res. 2016;4(4):354–65.
pubmed: 26880715 pmcid: 4884020 doi: 10.1158/2326-6066.CIR-15-0241
Khambholja K, Gehani M, Kothari R, Marulkar S. Data for: Prognostic value of tumor-associated regulatory T-cells as a biomarker in non-small cell lung cancer: a systematic review and meta-analysis. V2 ed. Harvard Dataverse; 2022. https://doi.org/10.7910/DVN/JQOI9V .

Auteurs

Kapil Khambholja (K)

Department of Medical Writing, Catalyst Clinical Research, 2528 Independence Blvd, Suite 100, Wilmington, NC, 28412, USA.

Manish Gehani (M)

Department of Biological Sciences, Birla Institute of Technology and Science, Pilani-Hyderabad Campus, Jawahar Nagar, Shameerpet Mandal, Hyderabad, Telangana, 500078, India. dr.manishgehani@gmail.com.

Rushabh Kothari (R)

Medical Oncology Department, Narayana Multispecialty Hospital, Opposite Police Station, Near Chakudiya Mahadev, Rakhial, Ahmedabad, Gujarat, 380023, India.

Sachin Marulkar (S)

Catalyst Clinical Research, 2528 Independence Blvd, Suite 100, Wilmington, NC, 28412, USA.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH