Changes in blood monocyte functional profile in breast cancer
Автор: Fedorov A.A., Prostakishina E.A., Patysheva M.R., Frolova A.A., Iamshchikov P.S., Larionova I.V., Stakheyeva M.N., Dorofeeva M.S., Bragina O.D., Choynzonov E.L., Kzhyshkowska J.G., Cherdyntseva N.V.
Журнал: Сибирский онкологический журнал @siboncoj
Рубрика: Лабораторные и экспериментальные исследования
Статья в выпуске: 6 т.21, 2022 года.
Бесплатный доступ
The purpose of the study was to identify functional features of circulation monocytes in patients with non-metastatic breast cancer. Material and Methods. The study cohort consisted of 10 breast cancer patients treated at Tomsk Cancer Research institute. 7 healthy female volunteers were enrolled as a control group. CD14+16-, CD14+16+ and CD14-16+ monocytes subsets were obtained from blood by sorting. Whole transcriptome profiling was provided in monocytes from patients and healthy females. Macrophages were differentiated from the obtained monocytes under in vitro conditions. The ability of conditioned media obtained from macrophages to influence apoptosis and proliferation of MDA-MB 231 cell line was evaluated. Results. Transcriptomic profiling revealed significant changes in monocytes of breast cancer patients. CD14+16- subset showed higher expression of transporters ABCA1 and ABCG1; chemokines CCR1, CRRL2, CXCR4; maturation and differentiation factors Mafb and Jun; endocytosis mediating factors CD163 and Siglec1; proteases and tetrasponins ADAM9, CD151, CD82, and growth factor HBEGF in patient group. Macrophages derived from monocytes of breast cancer patients produced factors that supported proliferation of the MDA-MB 231 cell line, which was not observed for monocytes from healthy volunteers. Conclusion. Thus, breast carcinoma has a systemic effect on peripheral blood monocytes, programming them to differentiate into macrophages with tumor supporting capacity.
Monocytes, tumor-associated macrophages, breast cancer, transcriptome, rna sequencing
Короткий адрес: https://sciup.org/140296696
IDR: 140296696 | DOI: 10.21294/1814-4861-2022-21-6-68-80
Список литературы Changes in blood monocyte functional profile in breast cancer
- Goldszmid R.S., Dzutsev A., Trinchieri G. Host immune response to infection and cancer: unexpected commonalities. Cell Host Microbe. 2014; 15(3): 295-305. https://doi.org/10.1016/j.chom.2014.02.003.
- Olingy C.E., Dinh H.Q., Hedrick C.C. Monocyte heterogeneity and functions in cancer. J Leukoc Biol. 2019; 106(2): 309-22. https://doi.org/10.1002/JLB.4RI0818-311R.
- Saqib U., Sarkar S., Suk K., Mohammad O., Baig M.S., Savai R. Phytochemicals as modulators of M1-M2 macrophages in infammation. Oncotarget. 2018; 9(25): 17937-50. https://doi.org/10.18632/oncotarget.24788.
- Larionova I., Tuguzbaeva G., Ponomaryova A., Stakheyeva M., Cherdyntseva N., Pavlov V., Choinzonov E., Kzhyshkowska J. Tumor-Associated Macrophages in Human Breast, Colorectal, Lung, Ovarian and Prostate Cancers. Front Oncol. 2020; 10. https://doi.org/10.3389/fonc.2020.566511.
- Ma W.T., Gao F., Gu K., Chen D.K. The Role of Monocytes and Macrophages in Autoimmune Diseases: A Comprehensive Review. Front Immunol. 2019; 10: 1140. https://doi.org/10.3389/fmmu.2019.01140.
- Ziegler-Heitbrock L., Ancuta P., Crowe S., Dalod M., Grau V., Hart D.N., Leenen P.J., Liu Y.J., MacPherson G., Randolph G.J., Scherberich J., Schmitz J., Shortman K., Sozzani S., Strobl H., Zembala M., Austyn J.M., Lutz M.B. Nomenclature of monocytes and dendritic cells in blood. Blood. 2010; 116(16): 74-80. https://doi.org/10.1182/blood-2010-02-258558.
- Kiss M., Caro A.A., Raes G., Laoui D. Systemic Reprogramming of Monocytes in Cancer. Front Oncol. 2020; 10: 1399. https://doi.org/10.3389/fonc.2020.01399.
- Poschke I., Mougiakakos D., Hansson J., Masucci G.V., Kiessling R. Immature immunosuppressive CD14+HLA-DR-/low cells in melanoma patients are Stat3hi and overexpress CD80, CD83, and DC-sign. Cancer Res. 2010; 70(11): 4335-45. https://doi.org/10.1158/0008-5472.CAN-09-3767.
- Hamm A., Prenen H., Van Delm W., Di Matteo M., Wenes M., Delamarre E., Schmidt T., Weitz J., Sarmiento R., Dezi A., Gasparini G., Rothé F., Schmitz R., D’Hoore A., Iserentant H., Hendlisz A., Mazzone M. Tumour-educated circulating monocytes are powerful candidate biomarkers for diagnosis and disease follow-up of colorectal cancer. Gut. 2016; 65(6): 990-1000. https://doi.org/10.1136/gutjnl-2014-308988.
- Cormican S., Griffn M.D. Human Monocyte Subset Distinctions and Function: Insights From Gene Expression Analysis. Front Immunol. 2020; 11: 1070. https://doi.org/10.3389/fmmu.2020.01070.
- Reuter J.A., Spacek D.V., Snyder M.P. High-throughput sequencing technologies. Mol Cell. 2015; 58(4): 586-97. https://doi.org/10.1016/j.molcel.2015.05.004.
- Chen S., Chai X., Wu X. Bioinformatical analysis of the key differentially expressed genes and associations with immune cell infltration in development of endometriosis. BMC Genom Data. 2022; 23(1): 20. https://doi.org/10.1186/s12863-022-01036-y.
- Kzhyshkowska J., Gudima A., Moganti K., Gratchev A., Orekhov A. Perspectives for Monocyte/Macrophage-Based Diagnostics of Chronic Inflammation. Transfus Med Hemother. 2016; 43(2): 66-77. https://doi.org/10.1159/000444943.
- Dobin A., Davis C.A., Schlesinger F., Drenkow J., Zaleski C., Jha S., Batut P., Chaisson M., Gingeras T.R. STAR: ultrafast universal RNA-seq aligner. Bioinformatics. 2013; 29(1): 15-21. https://doi.org/10.1093/bioinformatics/bts635.
- Hartley S.W., Mullikin J.C. QoRTs: a comprehensive toolset for quality control and data processing of RNA-Seq experiments. BMC Bioinformatics. 2015; 16(1): 224. https://doi.org/10.1186/s12859-015-0670-5.
- Xie Z., Bailey A., Kuleshov M.V., Clarke D.J.B., Evangelista J.E., Jenkins S.L., Lachmann A., Wojciechowicz M.L., Kropiwnicki E., Jagodnik K.M., Jeon M., Ma’ayan A. Gene Set Knowledge Discovery with Enrichr Curr Protoc. 2021; 1(3): 90. https://doi.org/10.1002/cpz1.90.
- Szklarczyk D., Gable A.L., Nastou K.C., Lyon D., Kirsch R., Pyysalo S., Doncheva N.T., Legeay M., Fang T., Bork P., Jensen L.J., von Mering C. The STRING database in 2021: customizable protein-protein networks, and functional characterization of user-uploaded gene/measure ment sets. Nucleic Acids Res. 2021; 49(D1): 605-12. https://doi.org/10.1093/nar/gkaa1074. Erratum in: Nucleic Acids Res. 2021; 49(18): 10800.
- Zenkova D. K.V., Sablina R., Artyomov M., Sergushichev A. Phantasus: visual and interactive gene expression analysis. 2018. https://doi.org/10.18129/B9.bioc.phantasus.
- Noy R., Pollard J.W. Tumor-associated macrophages: from mechanisms to therapy. Immunity. 2014; 41(1): 49-61. https://doi.org/10.1016/j.immuni.2014.06.010. Erratum in: Immunity. 2014; 41(5): 866.
- Cassetta L., Fragkogianni S., Sims A.H., Swierczak A., Forrester L.M., Zhang H., Soong D.Y.H., Cotechini T., Anur P., Lin E.Y., Fidanza A., LopezYrigoyen M., Millar M.R., Urman A., Ai Z., Spellman P.T., Hwang E.S., Dixon J.M., Wiechmann L., Coussens L.M., Smith H.O., Pollard J.W. Human Tumor-Associated Macrophage and Monocyte Transcriptional Landscapes Reveal Cancer-Specifc Reprogramming, Biomarkers, and Therapeutic Targets. Cancer Cell. 2019; 35(4): 588-602. https://doi.org/10.1016/j.ccell.2019.02.009.
- Ramos R.N., Rodriguez C., Hubert M., Ardin M., Treilleux I., Ries C.H., Lavergne E., Chabaud S., Colombe A., Trédan O., Guedes H.G., Laginha F., Richer W., Piaggio E., Barbuto J.A.M., Caux C., MénétrierCaux C., Bendriss-Vermare N. CD163+ tumor-associated macrophage accumulation in breast cancer patients refects both local diferentiation signals and systemic skewing of monocytes. Clin Transl Immunology. 2020; 9(2): 1108. https://doi.org/10.1002/cti2.1108.
- Patysheva M., Larionova I., Stakheyeva M., Grigoryeva E., Iamshchikov P., Tarabanovskaya N., Weiss C., Kardashova J., Frolova A., Rakina M., Prostakishina E., Zhuikova L., Cherdyntseva N., Kzhyshkowska J. Efect of Early-Stage Human Breast Carcinoma on Monocyte Programming. Front Oncol. 2022; 11. https://doi.org/10.3389/fonc.2021.800235.
- Sanford D.E., Belt B.A., Panni R.Z., Mayer A., Deshpande A.D., Carpenter D., Mitchem J.B., Plambeck-Suess S.M., Worley L.A., Goetz B.D., Wang-Gillam A., Eberlein T.J., Denardo D.G., Goedegebuure S.P., Linehan D.C. Infammatory monocyte mobilization decreases patient survival in pancreatic cancer: a role for targeting the CCL2/CCR2 axis. Clin Cancer Res. 2013; 19(13): 3404-15. https://doi.org/10.1158/1078-0432.CCR-13-0525.
- Pan Y.C., Jia Z.F., Cao D.H., Wu Y.H., Jiang J., Wen S.M., Zhao D., Zhang S.L., Cao X.Y. Preoperative lymphocyte-to-monocyte ratio (LMR) could independently predict overall survival of resectable gastric cancer patients. Medicine (Baltimore). 2018; 97(52). https://doi.org/10.1097/MD.0000000000013896.
- Lu C., Zhou L., Ouyang J., Yang H. Prognostic value of lymphocyte-to-monocyte ratio in ovarian cancer: A meta-analysis. Medicine (Baltimore). 2019; 98(24). https://doi.org/10.1097/MD.0000000000015876.
- Hayashi T., Fujita K., Tanigawa G., Kawashima A., Nagahara A., Ujike T., Uemura M., Takao T., Yamaguchi S., Nonomura N. Serum monocyte fraction of white blood cells is increased in patients with high Gleason score prostate cancer. Oncotarget. 2017; 8(21): 35255-61. https://doi.org/10.18632/oncotarget.13052.
- Rakina M.A. Kazakova E.O., Sudarskikh T.S., Bezgodova N.V., Villert A.B., Kolomiets L.A., Larionova I.V. Giant foam-like macrophages in advanced ovarian cancer. Siberian Journal of Oncology. 2022; 21(2): 45-54. https://doi.org/10.21294/1814-4861-2022-21-2-45-54.
- Fedorov A.A., Ermak N.A., Gerashchenko T.S., Topolnitskii E.B., Shefer N.A., Rodionov E.O., Stakheyeva M.N. Polarization of macrophages: mechanisms, markers and factors of induction. Siberian Journal of Oncology. 2022; 21(4): 124-36. https://doi.org/10.21294/1814-4861-2022-21-4-124-136.
- Jeong H., Hwang I., Kang S.H., Shin H.C., Kwon S.Y. TumorAssociated Macrophages as Potential Prognostic Biomarkers of Invasive Breast Cancer. J Breast Cancer. 2019; 22(1): 38-51. https://doi.org/10.4048/jbc.2019.22.e5.
- Tiainen S., Tumelius R., Rilla K., Hämäläinen K., Tammi M., Tammi R., Kosma V.M., Oikari S., Auvinen P. High numbers of macrophages, especially M2-like (CD163-positive), correlate with hyaluronan accumulation and poor outcome in breast cancer. Histopathology. 2015; 66(6): 873-83. https://doi.org/10.1111/his.12607.
- Miyasato Y., Shiota T., Ohnishi K., Pan C., Yano H., Horlad H., Yamamoto Y., Yamamoto-Ibusuki M., Iwase H., Takeya M., Komohara Y. High density of CD204-positive macrophages predicts worse clinical prognosis in patients with breast cancer. Cancer Sci. 2017; 108(8): 1693-700. https://doi.org/10.1111/cas.13287.
- Ge Z., Ding S. The Crosstalk Between Tumor-Associated Macrophages (TAMs) and Tumor Cells and the Corresponding Targeted Therapy. Front Oncol. 2020; 10. https://doi.org/10.3389/fonc.2020.590941.
- Chen Y., Song Y., Du W., Gong L., Chang H., Zou Z. Tumor-associated macrophages: an accomplice in solid tumor progression. J Biomed Sci. 2019; 26(1): 78. https://doi.org/10.1186/s12929-019-0568-z.
- Norton K.A., Jin K., Popel A.S. Modeling triple-negative breast cancer heterogeneity: Efects of stromal macrophages, fbroblasts and tumor vasculature. J Theor Biol. 2018; 452: 56-68. https://doi.org/10.1016/j.jtbi.2018.05.003.
- Eue I., Pietz B., Storck J., Klempt M., Sorg C. Transendothelial migration of 27E10+ human monocytes. Int Immunol. 2000; 12(11): 1593-604. https://doi.org/10.1093/intimm/12.11.1593.
- Viemann D., Strey A., Janning A., Jurk K., Klimmek K., Vogl T., Hirono K., Ichida F., Foell D., Kehrel B., Gerke V., Sorg C., Roth J. Myeloid-related proteins 8 and 14 induce a specifc infammatory response in human microvascular endothelial cells. Blood. 2005; 105(7): 2955-62. https://doi.org/10.1182/blood-2004-07-2520.
- Simkhes Yu.V., Karpov S.M., Baturin V.A., Vyshlova A. Role of s100 protein in the pathogenesis of pain syndromes. Neurology, Neuropsychiatry, Psychosomatics. 2016; 8(4): 62-4. https://doi.org/doi.org/10.14412/2074-2711-2016-4-62-64.
- Kim J.H., Oh S.H., Kim E.J., Park S.J., Hong S.P., Cheon J.H., Kim T.I., Kim W.H. The role of myofbroblasts in upregulation of S100A8 and S100A9 and the diferentiation of myeloid cells in the colorectal cancer microenvironment. Biochem Biophys Res Commun. 2012; 423(1): 60-6. https://doi.org/10.1016/j.bbrc.2012.05.081.
- Fox J.M., Kausar F., Day A., Osborne M., Hussain K., Mueller A., Lin J., Tsuchiya T., Kanegasaki S., Pease J.E. CXCL4/Platelet Factor 4 is an agonist of CCR1 and drives human monocyte migration. Scientifc reports. 2018; 8(1): 9466. https://doi.org/10.1038/s41598-018-27710-9.
- Schioppa T., Sozio F., Barbazza I., Scutera S., Bosisio D., Sozzani S., Del Prete A. Molecular Basis for CCRL2 Regulation of Leukocyte Migration. Front Cell Dev Biol. 2020; 8. https://doi.org/10.3389/fcell.2020.615031.
- Jayasingam S.D., Citartan M., Thang T.H., Mat Zin A.A., Ang K.C., Ch’ng E.S. Evaluating the Polarization of Tumor-Associated Macrophages Into M1 and M2 Phenotypes in Human Cancer Tissue: Technicalities and Challenges in Routine Clinical Practice. Front Oncol. 2020; 9: 1512. https://doi.org/10.3389/fonc.2019.01512.
- Fontana M.F., Baccarella A., Pancholi N., Pufall M.A., Herbert D.R., Kim C.C. JUNB is a key transcriptional modulator of macrophage activation. J Immunol. 2015; 194(1): 177-86. https://doi.org/10.4049/jimmunol.1401595.
- Hamada M., Tsunakawa Y., Jeon H., Yadav M.K., Takahashi S. Role of MafB in macrophages. Exp Anim. 2020; 69(1): 1-10. https://doi.org/10.1538/expanim.19-0076.
- Rigo A., Gottardi M., Zamò A., Mauri P., Bonifacio M., Krampera M., Damiani E., Pizzolo G., Vinante F. Macrophages may promote cancer growth via a GM-CSF/HB-EGF paracrine loop that is enhanced by CXCL12. Mol Cancer. 2010; 9: 273. https://doi.org/10.1186/1476-4598-9-273.
- Vlaicu P., Mertins P., Mayr T., Widschwendter P., Ataseven B., Högel B., Eiermann W., Knyazev P., Ullrich A. Monocytes/macrophages support mammary tumor invasivity by co-secreting lineage-specifc EGFR ligands and a STAT3 activator. BMC Cancer. 2013; 13: 197. https://doi.org/10.1186/1471-2407-13-197.
- Ongusaha P.P., Kwak J.C., Zwible A.J., Macip S., Higashiyama S., Taniguchi N., Fang L., Lee S.W. HB-EGF is a potent inducer of tumor growth and angiogenesis. Cancer Res. 2004; 64(15): 5283-90. https://doi.org/10.1158/0008-5472.CAN-04-0925.
- Carroll M.J., Kapur A., Felder M., Patankar M.S., Kreeger P.K. M2 macrophages induce ovarian cancer cell proliferation via a heparin binding epidermal growth factor/matrix metalloproteinase 9 intercellular feedback loop. Oncotarget. 2016; 7(52): 86608-20. https://doi.org/10.18632/oncotarget.13474.
- Yonemitsu K., Miyasato Y., Shiota T., Shinchi Y., Fujiwara Y., Hosaka S., Yamamoto Y., Komohara Y. Soluble Factors Involved in Cancer Cell-Macrophage Interaction Promote Breast Cancer Growth. Anticancer Res. 2021; 41(9): 4249-58. https://doi.org/10.21873/anticanres.15229.
- Yu X., Zhang Q., Zhang X., Han Q., Li H., Mao Y., Wang X., Guo H., Irwin D.M., Niu G., Tan H. Exosomes from Macrophages Exposed to Apoptotic Breast Cancer Cells Promote Breast Cancer Proliferation and Metastasis. J Cancer. 2019; 10(13): 2892-2906. https://doi.org/10.7150/jca.31241.
- Wu D.M., Wen X., Han X.R., Wang S., Wang Y.J., Shen M., Fan S.H., Zhang Z.F., Shan Q., Li M.Q., Hu B., Lu J., Chen G.Q., Zheng Y.L. Bone Marrow Mesenchymal Stem Cell-Derived Exosomal MicroRNA-126 -3p Inhibits Pancreatic Cancer Development by Targeting ADAM9. Mol Ther Nucleic Acids. 2019; 16: 229-45. https://doi.org/10.1016/j.omtn.2019.02.022. Retraction in: Mol Ther Nucleic Acids. 2022; 29: 617.
- Zhao K., Wang Z., Hackert T., Pitzer C., Zöller M. Tspan8 and Tspan8/CD151 knockout mice unravel the contribution of tumor and host exosomes to tumor progression. J Exp Clin Cancer Res. 2018; 37(1): 312. https://doi.org/10.1186/s13046-018-0961-6.
- Xiao D., Dong Z., Zhen L., Xia G., Huang X., Wang T., Guo H., Yang B., Xu C., Wu W., Zhao X., Xu H. Combined Exosomal GPC1, CD82, and Serum CA19-9 as Multiplex Targets: A Specifc, Sensitive, and Reproducible Detection Panel for the Diagnosis of Pancreatic Cancer. Mol Cancer Res. 2020; 18(2): 300-10. https://doi.org/10.1158/1541-7786.MCR-19-0588.
- Yunusova N.V., Zambalova E.A., Patysheva M.R., Kolegova E.S., Afanas’ev S.G., Cheremisina O.V., Grigor’eva A.E., Tamkovich S.N., Kondakova I.V. Exosomal Protease Cargo as Prognostic Biomarker in Colorectal Cancer. Asian Pac J Cancer Prev. 2021; 22(3): 861-9. https://doi.org/10.31557/APJCP.2021.22.3.861.