Chemotherapy-induced developmental trajectories of monocytes in breast cancer
- 作者: Gerashchenko T.S.1, Patysheva M.R.1, Fedorenko A.A.1,2, Filatova A.P.1, Vostrikova M.A.1, Bragina O.D.1, Fedorov A.A.1, Iamshchikov P.S.1, Denisov E.V.1
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隶属关系:
- Tomsk National Research Medical Center, Russian Academy of Sciences
- National Research Tomsk State University
- 期: 卷 28, 编号 4 (2024): ONCOLOGY
- 页面: 427-438
- 栏目: ONCOLOGY
- URL: https://journal-vniispk.ru/2313-0245/article/view/319736
- DOI: https://doi.org/10.22363/2313-0245-2024-28-4-427-438
- EDN: https://elibrary.ru/GNCAUM
- ID: 319736
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Relevance . Monocytes are circulating immune cells which are traditionally divided into three subsets. The contribution of each subset to breast cancer pathogenesis is controversial. Moreover, there is no data regarding the programming of monocyte subsets towards antitumor activity induced by chemotherapy. Aim . To study the trajectories of monocyte subsets and transcriptomic changes in blood monocytes during neoadjuvant chemotherapy (NAC). Materials and Methods . Mononuclear cells were purified from the peripheral blood of nine triple-negative breast cancer (TNBC) patients before NAC and on the 3rd and 21st day after the first NAC cycle (AC regimen). Total cell concentration and viability (Calcein/DRAQ7) were assessed by flow cytometry. Single-cell RNA sequencing was performed on a Genolab M platform (GeneMind Biosciences) using the 10x Genomics technology for fixed samples. Data were analyzed using Seurat, SingleR, and the dynverse R package for trajectories. Results and Discussion . The trajectory analysis indicated that monocytes were clustered into three subsets: classical, non-classical, and intermediate. Classical monocytes were characterized by high expression of CD14 , CSF3R , S100A8 , S100A9 , VCAN , LYZ , SELL , and GRN genes, whereas non-classical monocytes expressed FCGR3A , MTSS1 , TCF7L2 , CSF1R , SPN , EVL , and LYN . The developmental trajectories of monocytes were significantly affected by chemotherapy. Transcriptionally, classical monocytes were subdivided into two clusters: one characterized by proliferative signals and the other by stress signals. By day 21st after NAC, developmental trajectories of monocytes and their subset composition were observed to recover. Chemotherapy promoted the pro-inflammatory activity of monocytes. Conclusion . Peripheral blood monocytes of TNBC patients are capable of recovering their subset composition after NAC by the 21st day after the first cycle of chemotherapy.
作者简介
Tatiana Gerashchenko
Tomsk National Research Medical Center, Russian Academy of Sciences
编辑信件的主要联系方式.
Email: t_gerashchenko@oncology.tomsk.ru
ORCID iD: 0000-0002-7283-0092
SPIN 代码: 7900-9700
Tomsk, Russian Federation
Marina Patysheva
Tomsk National Research Medical Center, Russian Academy of Sciences
Email: t_gerashchenko@oncology.tomsk.ru
ORCID iD: 0000-0003-2865-7576
SPIN 代码: 5714-4611
Tomsk, Russian Federation
Anastasia Fedorenko
Tomsk National Research Medical Center, Russian Academy of Sciences; National Research Tomsk State University
Email: t_gerashchenko@oncology.tomsk.ru
ORCID iD: 0000-0003-3297-1680
SPIN 代码: 8092-0070
Tomsk, Russian Federation
Anastasia Filatova
Tomsk National Research Medical Center, Russian Academy of Sciences
Email: t_gerashchenko@oncology.tomsk.ru
ORCID iD: 0000-0002-0693-2314
Tomsk, Russian Federation
Maria Vostrikova
Tomsk National Research Medical Center, Russian Academy of Sciences
Email: t_gerashchenko@oncology.tomsk.ru
ORCID iD: 0000-0002-0256-5342
Tomsk, Russian Federation
Olga Bragina
Tomsk National Research Medical Center, Russian Academy of Sciences
Email: t_gerashchenko@oncology.tomsk.ru
ORCID iD: 0000-0001-5281-7758
SPIN 代码: 7961-5918
Tomsk, Russian Federation
Anton Fedorov
Tomsk National Research Medical Center, Russian Academy of Sciences
Email: t_gerashchenko@oncology.tomsk.ru
ORCID iD: 0000-0002-5121-2535
SPIN 代码: 1315-8100
Tomsk, Russian Federation
Pavel Iamshchikov
Tomsk National Research Medical Center, Russian Academy of Sciences
Email: t_gerashchenko@oncology.tomsk.ru
ORCID iD: 0000-0002-0646-6093
SPIN 代码: 9624-3257
Tomsk, Russian Federation
Evgeny Denisov
Tomsk National Research Medical Center, Russian Academy of Sciences
Email: t_gerashchenko@oncology.tomsk.ru
ORCID iD: 0000-0003-2923-9755
SPIN 代码: 9498-5797
Tomsk, Russian Federation
参考
- Guilliams M, Mildner A, Yona S. Developmental and Functional Heterogeneity of Monocytes. Immunity. 2018;49(4):595–613. doi: 10.1016/j.immuni.2018.10.005
- Grinberg MV, Lokhonina AV, Vishnyakova PA, Makarov AV, Kananykhina EY, Eremina IZ, Glinkina VV, Elchaninov AV, Fatkhudinov TK. Migration, proliferation and cell death of regenerating liver macrophages in an experimental model. RUDN Journal of Medicine. 2023;27(4):449–458. doi: 10.22363/2313-0245-2023-27-4-449-458
- Patysheva M, Frolova A, Larionova I, Afanas’ev S, Tarasova A, Cherdyntseva N, Kzhyshkowska J. Monocyte programming by cancer therapy. Frontiers in immunology. 2022;13:994319. doi: 10.3389/fimmu.2022.994319
- Ugel S, Canè S, De Sanctis F, Bronte V. Monocytes in the Tumor Microenvironment. Annual review of pathology. 2021;16:93–122. doi: 10.1146/annurev-pathmechdis-012418-013058
- Ziegler-Heitbrock L, Ancuta P, Crowe S, Dalod M, Grau V, Hart DN, Leenen PJ, Liu YJ, MacPherson G, Randolph GJ, Scherberich J, Schmitz J, Shortman K, Sozzani S, Strobl H, Zembala M, Austyn JM, Lutz MB. Nomenclature of monocytes and dendritic cells in blood. Blood. 2010;116(16): e74–80. doi: 10.1182/blood-2010-02-258558
- Wong KL, Tai JJ, Wong WC, Han H, Sem X, Yeap WH, Kourilsky P, Wong SC. Gene expression profiling reveals the defining features of the classical, intermediate, and nonclassical human monocyte subsets. Blood. 2011;118(5): e16–31. doi: 10.1182/blood-2010-12-326355
- Anbazhagan K, Duroux-Richard I, Jorgensen C, Apparailly F. Transcriptomic network support distinct roles of classical and non-classical monocytes in human. International reviews of immunology. 2014;33(6):470–89. doi: 10.3109/08830185.2014.902453
- Buscher K, Marcovecchio P, Hedrick CC, Ley K. Patrolling Mechanics of Non-Classical Monocytes in Vascular Inflammation. Frontiers in cardiovascular medicine. 2017;4:80. doi: 10.3389/fcvm.2017.00080
- Olingy CE, Dinh HQ, Hedrick CC. Monocyte heterogeneity and functions in cancer. Journal of leukocyte biology. 2019;106(2):309–322. doi: 10.1002/jlb.4ri0818-311r
- Wang R, Bao W, Pal M, Liu Y, Yazdanbakhsh K, Zhong H. Intermediate monocytes induced by IFN-γ inhibit cancer metastasis by promoting NK cell activation through FOXO1 and interleukin‑27. Journal for immunotherapy of cancer. 2022;10(1) doi: 10.1136/jitc-2021-003539
- Kiss M, Caro AA, Raes G, Laoui D. Systemic Reprogramming of Monocytes in Cancer. Frontiers in oncology. 2020;10:1399. doi: 10.3389/fonc.2020.01399
- Gamrekelashvili J, Giagnorio R, Jussofie J, Soehnlein O, Duchene J, Briseño CG, Ramasamy SK, Krishnasamy K, Limbourg A, Kapanadze T, Ishifune C, Hinkel R, Radtke F, Strobl LJ, Zimber-Strobl U, Napp LC, Bauersachs J, Haller H, Yasutomo K, Kupatt C, Murphy KM, Adams RH, Weber C, Limbourg FP. Regulation of monocyte cell fate by blood vessels mediated by Notch signalling. Nature communications. 2016;7:12597. doi: 10.1038/ncomms12597
- Miyake K, Ito J, Takahashi K, Nakabayashi J, Brombacher F, Shichino S, Yoshikawa S, Miyake S, Karasuyama H. Single-cell transcriptomics identifies the differentiation trajectory from inflammatory monocytes to pro-resolving macrophages in a mouse skin allergy model. Nature communications. 2024;15(1):1666. doi: 10.1038/s41467-024-46148-4
- Narasimhan PB, Marcovecchio P, Hamers AAJ, Hedrick CC. Nonclassical Monocytes in Health and Disease. Annual review of immunology. 2019;37:439–456. doi: 10.1146/annurev-immunol-042617-053119
- Ohkuma R, Fujimoto Y, Ieguchi K, Onishi N, Watanabe M, Takayanagi D, Goshima T, Horiike A, Hamada K, Ariizumi H, Hirasawa Y, Ishiguro T, Suzuki R, Iriguchi N, Tsurui T, Sasaki Y, Homma M, Yamochi T, Yoshimura K, Tsuji M, Kiuchi Y, Kobayashi S, Tsunoda T, Wada S. Monocyte subsets associated with the efficacy of anti-PD‑1 antibody monotherapy. Oncology letters. 2023;26(3):381. doi: 10.3892/ol.2023.13967
- Hanna RN, Cekic C, Sag D, Tacke R, Thomas GD, Nowyhed H, Herrley E, Rasquinha N, McArdle S, Wu R, Peluso E, Metzger D, Ichinose H, Shaked I, Chodaczek G, Biswas SK, Hedrick CC. Patrolling monocytes control tumor metastasis to the lung. Science (New York, NY). 2015;350(6263):985–90. doi: 10.1126/science.aac9407
- Hao Y, Stuart T, Kowalski MH, Choudhary S, Hoffman P, Hartman A, Srivastava A, Molla G, Madad S, Fernandez-Granda C, Satija R. Dictionary learning for integrative, multimodal and scalable single-cell analysis. Nature biotechnology. 2024;42(2):293–304. doi: 10.1038/s41587-023-01767-y
- Cannoodt R. Inferring, interpreting and visualising trajectories using a streamlined set of packages. March 29, 2019. https://dynverse.github.io/dyno. Accessed February 13, 2024.
- Ożańska A, Szymczak D, Rybka J. Pattern of human monocyte subpopulations in health and disease. Scandinavian journal of immunology. 2020;92(1): e12883. doi: 10.1111/sji.12883
- Schauer D, Starlinger P, Reiter C, Jahn N, Zajc P, Buchberger E, Bachleitner-Hofmann T, Bergmann M, Stift A, Gruenberger T, Brostjan C. Intermediate monocytes but not TIE2‑expressing monocytes are a sensitive diagnostic indicator for colorectal cancer. PloS one. 2012;7(9): e44450. doi: 10.1371/journal.pone.0044450
- Subimerb C, Pinlaor S, Lulitanond V, Khuntikeo N, Okada S, McGrath MS, Wongkham S. Circulating CD14(+) CD16(+) monocyte levels predict tissue invasive character of cholangiocarcinoma. Clinical and experimental immunology. 2010;161(3):471–9. doi: 10.1111/j.1365-2249.2010.04200.x
- Metcalf TU, Wilkinson PA, Cameron MJ, Ghneim K, Chiang C, Wertheimer AM, Hiscott JB, Nikolich-Zugich J, Haddad EK. Human Monocyte Subsets Are Transcriptionally and Functionally Altered in Aging in Response to Pattern Recognition Receptor Agonists. Journal of immunology (Baltimore, Md: 1950). 2017;199(4):1405–1417. doi: 10.4049/jimmunol.1700148
- Ito Y, Nakahara F, Kagoya Y, Kurokawa M. CD62L expression level determines the cell fate of myeloid progenitors. Stem cell reports. 2021;16(12):2871–2886. doi: 10.1016/j.stemcr.2021.10.012
- Patel AA, Zhang Y, Fullerton JN, Boelen L, Rongvaux A, Maini AA, Bigley V, Flavell RA, Gilroy DW, Asquith B, Macallan D, Yona S. The fate and lifespan of human monocyte subsets in steady state and systemic inflammation. The Journal of experimental medicine. 2017;214(7):1913–1923. doi: 10.1084/jem.20170355
- Geller MA, Bui-Nguyen TM, Rogers LM, Ramakrishnan S. Chemotherapy induces macrophage chemoattractant protein‑1 production in ovarian cancer. International journal of gynecological cancer: official journal of the International Gynecological Cancer Society. 2010;20(6):918–25. doi: 10.1111/IGC.0b013e3181e5c442
- Dijkgraaf EM, Heusinkveld M, Tummers B, Vogelpoel LT, Goedemans R, Jha V, Nortier JW, Welters MJ, Kroep JR, van der Burg SH. Chemotherapy alters monocyte differentiation to favor generation of cancer-supporting M2 macrophages in the tumor microenvironment. Cancer research. 2013;73(8):2480–92. doi: 10.1158/0008-5472.can-12-3542
- Valdés-Ferrada J, Muñoz-Durango N, Pérez-Sepulveda A, Muñiz S, Coronado-Arrázola I, Acevedo F, Soto JA, Bueno SM, Sánchez C, Kalergis AM. Peripheral Blood Classical Monocytes and Plasma Interleukin 10 Are Associated to Neoadjuvant Chemotherapy Response in Breast Cancer Patients. Frontiers in immunology. 2020;11:1413. doi: 10.3389/fimmu.2020.01413
- Friedlová N, Zavadil Kokáš F, Hupp TR, Vojtěšek B, Nekulová M. IFITM protein regulation and functions: Far beyond the fight against viruses. Frontiers in immunology. 2022;13:1042368. doi: 10.3389/fimmu.2022.1042368
- Sheng G, Chu H, Duan H, Wang W, Tian N, Liu D, Sun H, Sun Z. LRRC25 Inhibits IFN-γ Secretion by Microglia to Negatively Regulate Anti-Tuberculosis Immunity in Mice. Microorganisms. 2023;11(10). doi: 10.3390/microorganisms11102500
- Juric V, Mayes E, Binnewies M, Lee T, Canaday P, Pollack JL, Rudolph J, Du X, Liu VM, Dash S, Palmer R, Jahchan NS, Ramoth Å J, Lacayo S, Mankikar S, Norng M, Brassell C, Pal A, Chan C, Lu E, Sriram V, Streuli M, Krummel MF, Baker KP, Liang L. TREM1 activation of myeloid cells promotes antitumor immunity. Science translational medicine. 2023;15(711): eadd9990. doi: 10.1126/scitranslmed.add9990
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