Myeloid‑derived suppressor cells as targets of emerging therapies and nanotherapies (Review)
- Authors:
- Dileep Kumar
- Victor Carlos Da Silva
- Natalia Lemos Chaves
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Affiliations: Department of Genetics and Morphology, Institutes of Biological Sciences, University of Brasilia, Brasilia, DF 70910‑900, Brazil, Microscopy and Microanalysis Laboratory, Institutes of Biological Sciences, University of Brasilia, Brasilia, DF 70910‑900, Brazil - Published online on: June 25, 2024 https://doi.org/10.3892/mi.2024.170
- Article Number: 46
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Copyright : © Kumar et al. This is an open access article distributed under the terms of Creative Commons Attribution License [CC BY 4.0].
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Abstract
Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA and Jemal A: Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 68:394–424. 2018.PubMed/NCBI View Article : Google Scholar | |
Lei S, Zheng R, Zhang S, Wang S, Chen R, Sun K, Zeng H, Zhou J and Wei W: Global patterns of breast cancer incidence and mortality: A population-based cancer registry data analysis from 2000 to 2020. Cancer Commun (Lond). 41:1183–1194. 2021.PubMed/NCBI View Article : Google Scholar | |
Gradishar WJ, Moran MS, Abraham J, Aft R, Agnese D, Allison KH, Anderson B, Burstein HJ, Chew H, Dang C, et al: Breast cancer, version 3.2022, NCCN clinical practice guidelines in oncology. J Natl Compr Canc Netw. 20:691–722. 2022.PubMed/NCBI View Article : Google Scholar | |
Partridge AH, Burstein HJ and Winer EP: Side effects of chemotherapy and combined chemohormonal therapy in women with early-stage breast cancer. J Natl Cancer Inst Monogr. (30):135–142. 2001.PubMed/NCBI View Article : Google Scholar | |
Langeh U, Kumar V, Ahuja P, Singh C and Singh A: An update on breast cancer chemotherapy-associated toxicity and their management approaches. Health Sci Re. 9(100119)2023. | |
Slamon D, Eiermann W, Robert N, Pienkowski T, Martin M, Press M, Mackey J, Glaspy J, Chan A, Pawlicki M, et al: Adjuvant trastuzumab in HER2-positive breast cancer. N Engl J Med. 365:1273–1283. 2011.PubMed/NCBI View Article : Google Scholar | |
Darby SC, Ewertz M, McGale P, Bennet AM, Blom-Goldman U, Brønnum D, Correa C, Cutter D, Gagliardi G, Gigante B, et al: Risk of ischemic heart disease in women after radiotherapy for breast cancer. N Engl J Med. 368:987–998. 2013.PubMed/NCBI View Article : Google Scholar | |
Adams S, Gatti-Mays ME, Kalinsky K, Korde LA, Sharon E, Amiri-Kordestani L, Bear H, McArthur HL, Frank E, Perlmutter J, et al: Current landscape of immunotherapy in breast cancer: A review. JAMA Oncol. 5:1205–1214. 2019.PubMed/NCBI View Article : Google Scholar | |
Verheijden RJ, van Eijs MJM, May AM, van Wijk F and Suijkerbuijk KPM: Immunosuppression for immune-related adverse events during checkpoint inhibition: An intricate balance. NPJ Precis Oncol. 7(41)2023.PubMed/NCBI View Article : Google Scholar | |
Martins F, Sofiya L, Sykiotis GP, Lamine F, Maillard M, Fraga M, Shabafrouz K, Ribi C, Cairoli A, Guex-Crosier Y, et al: Adverse effects of immune-checkpoint inhibitors: epidemiology, management and surveillance. Nat Rev Clin Oncol. 6:563–580. 2019.PubMed/NCBI View Article : Google Scholar | |
Trimboli RM, Giorgi Rossi P, Battisti NML, Cozzi A, Magni V, Zanardo M and Sardanelli F: Do we still need breast cancer screening in the era of targeted therapies and precision medicine? Insights Imaging. 11(105)2020.PubMed/NCBI View Article : Google Scholar | |
Elemam NM, Talaat IM, Assal RA and Youness RA: Understanding the crosstalk between immune cells and the tumor microenvironment in cancer and its implications for immunotherapy. Front Med (Lausanne). 10(1202581)2023.PubMed/NCBI View Article : Google Scholar | |
Cha YJ and Koo JS: Role of tumor-associated myeloid cells in breast cancer. Cells. 9(1785)2020.PubMed/NCBI View Article : Google Scholar | |
Ortiz ML, Lu L, Ramachandran I and Gabrilovich DI: Myeloid-derived suppressor cells in the development of lung cancer. Cancer Immunol Res. 2:50–58. 2014.PubMed/NCBI View Article : Google Scholar | |
Srivastava MK, Zhu L, Harris-White M, Kar UK, Huang M, Johnson MF, Lee JM, Elashoff D, Strieter R, Dubinett S and Sharma S: Myeloid suppressor cell depletion augments antitumor activity in lung cancer. PLoS One. 7(e40677)2012.PubMed/NCBI View Article : Google Scholar | |
Yang Z, Guo J, Weng L, Tang W, Jin S and Ma W: Myeloid-derived suppressor cells-new and exciting players in lung cancer. J Hematol Oncol. 13(10)2020.PubMed/NCBI View Article : Google Scholar | |
Blaye C, Boyer T, Peyraud F, Domblides C and Larmonier N: Beyond immunosuppression: The multifaceted functions of tumor-promoting myeloid cells in breast cancers. Front Immunol. 13(838040)2022.PubMed/NCBI View Article : Google Scholar | |
Li L, Li M and Jia Q: Myeloid-derived suppressor cells: Key immunosuppressive regulators and therapeutic targets in cancer. Pathol Res Pract. 248(154711)2023.PubMed/NCBI View Article : Google Scholar | |
Parker KH, Beury DW and Ostrand-Rosenberg S: Myeloid-derived suppressor cells: critical cells driving immune suppression in the tumor microenvironment. Adv Cancer Res. 128:95–139. 2015.PubMed/NCBI View Article : Google Scholar | |
Bronte V, Brandau S, Chen SH, Colombo MP, Frey AB, Greten TF, Mandruzzato S, Murray PJ, Ochoa A, Ostrand-Rosenberg S, et al: Recommendations for myeloid-derived suppressor cell nomenclature and characterization standards. Nat Commun. 7(12150)2016.PubMed/NCBI View Article : Google Scholar | |
Cassetta L, Baekkevold ES, Brandau S, Bujko A, Cassatella MA, Dorhoi A, Krieg C, Lin A, Loré K, Marini O, et al: Deciphering myeloid-derived suppressor cells: isolation and markers in humans, mice, and non-human primates. Cancer Immunol Immunother. 68:687–697. 2019.PubMed/NCBI View Article : Google Scholar | |
Wang PF, Song SY, Wang TJ, Ji WJ, Li SW, Liu N and Yan CX: Prognostic role of pretreatment circulating MDSCs in patients with solid malignancies: A meta-analysis of 40 studies. Oncoimmunology. 7(e1494113)2018.PubMed/NCBI View Article : Google Scholar | |
Condamine T, Mastio J and Gabrilovich DI: Transcriptional regulation of myeloid-derived suppressor cells. J Leukoc Biol. 98:913–922. 2015.PubMed/NCBI View Article : Google Scholar | |
Alshetaiwi H, Pervolarakis N, McIntyre LL, Ma D, Nguyen Q, Rath JA, Nee K, Hernandez G, Evans K, Torosian L, et al: Defining the emergence of myeloid-derived suppressor cells in breast cancer using single-cell transcriptomics. Sci Immunol. 5(eaay6017)2020.PubMed/NCBI View Article : Google Scholar | |
Millrud CR, Bergenfelz C and Leandersson K: On the origin of myeloid-derived suppressor cells. Oncotarget. 8:3649–3665. 2017.PubMed/NCBI View Article : Google Scholar | |
Sun HW, Wu WC, Chen HT, Xu YT, Yang YY, Chen J, Yu XJ, Wang Z, Shuang ZY and Zheng L: Glutamine deprivation promotes the generation and mobilization of MDSCs by enhancing expression of G-CSF and GM-CSF. Front Immunol. 11(616367)2021.PubMed/NCBI View Article : Google Scholar | |
Rong Y, Yuan CH, Qu Z, Zhou H, Guan Q, Yang N, Leng XH, Bu L, Wu K and Wang F: Doxorubicin-resistant cancer cells activate myeloid-derived suppressor cells by releasing PGE2. Sci Rep. 6(23824)2016.PubMed/NCBI View Article : Google Scholar | |
Ching MM, Reader J and Fulton AM: Eicosanoids in cancer: prostaglandin E2 receptor 4 in cancer therapeutics and immunotherapy. Front Pharmacol. 11(530199)2020.PubMed/NCBI View Article : Google Scholar | |
Pradhan AK, Maji S, Bhoopathi P, Talukdar S, Mannangatti P, Guo C, Wang XY, Cartagena LC, Idowu M, Landry JW, et al: Pharmacological inhibition of MDA-9/Syntenin blocks breast cancer metastasis through suppression of IL-1β. Proc Natl Acad Sci USA. 118(e2103180118)2021.PubMed/NCBI View Article : Google Scholar | |
Jiang M, Chen J, Zhang W, Zhang R, Ye Y, Liu P, Yu W, Wei F, Ren X and Yu J: Interleukin-6 trans-signaling pathway promotes immunosuppressive myeloid-derived suppressor cells via suppression of suppressor of cytokine signaling 3 in breast cancer. Front Immunol. 8(1840)2017.PubMed/NCBI View Article : Google Scholar | |
Zhao N, Zhu W, Wang J, Liu W, Kang L, Yu R and Liu B: Group 2 innate lymphoid cells promote TNBC lung metastasis via the IL-13-MDSC axis in a murine tumor model. Int Immunopharmacol. 99(107924)2021.PubMed/NCBI View Article : Google Scholar | |
Popović M, Dedić Plavetić N, Vrbanec D, Marušić Z, Mijatović D and Kulić A: Interleukin 17 in early invasive breast cancer. Front Oncol. 13(1171254)2023.PubMed/NCBI View Article : Google Scholar | |
Gao W, Wen H, Liang L, Dong X, Du R, Zhou W, Zhang X, Zhang C, Xiang R and Li N: IL20RA signaling enhances stemness and promotes the formation of an immunosuppressive microenvironment in breast cancer. Theranostics. 11:2564–2580. 2021.PubMed/NCBI View Article : Google Scholar | |
Xiao P, Wan X, Cui B, Liu Y, Qiu C, Rong J, Zheng M, Song Y, Chen L, He J, et al: Interleukin 33 in tumor microenvironment is crucial for the accumulation and function of myeloid-derived suppressor cells. Oncoimmunology. 5(e1063772)2016.PubMed/NCBI View Article : Google Scholar | |
Kajihara N, Kobayashi T, Otsuka R, Nio-Kobayashi J, Oshino T, Takahashi M, Imanishi S, Hashimoto A, Wada H and Seino KI: Tumor-derived interleukin-34 creates an immunosuppressive and chemoresistant tumor microenvironment by modulating myeloid-derived suppressor cells in triple-negative breast cancer. Cancer Immunol Immunother. 72:851–864. 2023.PubMed/NCBI View Article : Google Scholar | |
Simpson KD, Templeton DJ and Cross JV: Macrophage migration inhibitory factor promotes tumor growth and metastasis by inducing myeloid-derived suppressor cells in the tumor microenvironment. J Immunol. 189:5533–5540. 2012.PubMed/NCBI View Article : Google Scholar | |
Liu QW, Chen Y, Li JY, Xiao L, Zhang WJ, Zhao JL, Gu HC, Wu HY, Zuo GS, Deng KY and Xin HB: Bone marrow cells are differentiated into MDSCs by BCC-Ex through down-regulating the expression of CXCR4 and activating the STAT3 signalling pathway. J Cell Mol Med. 25:5497–5510. 2021.PubMed/NCBI View Article : Google Scholar | |
Mundy-Bosse BL, Thornton LM, Yang HC, Andersen BL and Carson WE: Psychological stress is associated with altered levels of myeloid-derived suppressor cells in breast cancer patients. Cell Immunol. 270:80–87. 2011.PubMed/NCBI View Article : Google Scholar | |
He K, Liu X, Hoffman RD, Shi RZ, Lv GY and Gao JL: G-CSF/GM-CSF-induced hematopoietic dysregulation in the progression of solid tumors. FEBS Open Bio. 12:1268–1285. 2022.PubMed/NCBI View Article : Google Scholar | |
Smith KG and Clatworthy MR: FcγRIIB in autoimmunity and infection: Evolutionary and therapeutic implications. Nat Rev Immunol. 10:328–343. 2010.PubMed/NCBI View Article : Google Scholar | |
Wu L, Xu Y, Zhao H, Zhou Y, Chen Y, Yang S, Lei J, Zhang J, Wang J, Wu Y and Li Y: FcγRIIB potentiates differentiation of myeloid-derived suppressor cells to mediate tumor immunoescape. Theranostics. 12:842–858. 2022.PubMed/NCBI View Article : Google Scholar | |
Hillmer EJ, Zhang H, Li HS and Watowich SS: STAT3 signaling in immunity. Cytokine Growth Factor Rev. 31:1–15. 2016.PubMed/NCBI View Article : Google Scholar | |
Liao WC, Yen HR, Chen CH, Chu YH, Song YC, Tseng TJ and Liu CH: CHPF promotes malignancy of breast cancer cells by modifying syndecan-4 and the tumor microenvironment. Am J Cancer Res. 11:812–826. 2021.PubMed/NCBI | |
Liu C, Qiang J, Deng Q, Xia J, Deng L, Zhou L, Wang D, He X, Liu Y, Zhao B, et al: ALDH1A1 activity in tumor-initiating cells remodels myeloid-derived suppressor cells to promote breast cancer progression. Cancer Res. 81:5919–5934. 2021.PubMed/NCBI View Article : Google Scholar | |
Jiang M, Zhang W, Zhang R, Liu P, Ye Y, Yu W, Guo X and Yu J: Cancer exosome-derived miR-9 and miR-181a promote the development of early-stage MDSCs via interfering with SOCS3 and PIAS3 respectively in breast cancer. Oncogene. 39:4681–4694. 2020.PubMed/NCBI View Article : Google Scholar | |
Zhang W, Jiang M, Chen J, Zhang R, Ye Y, Liu P, Yu W and Yu J: SOCS3 suppression promoted the recruitment of CD11b+ Gr-1-F4/80-MHCII-early-stage myeloid-derived suppressor cells and accelerated interleukin-6-related tumor invasion via affecting myeloid differentiation in breast cancer. Front Immunol. 9(1699)2018.PubMed/NCBI View Article : Google Scholar | |
Welte T, Kim IS, Tian L, Gao X, Wang H, Li J, Holdman XB, Herschkowitz JI, Pond A, Xie G, et al: Oncogenic mTOR signalling recruits myeloid-derived suppressor cells to promote tumour initiation. Nat Cell Biol. 18:632–644. 2016.PubMed/NCBI View Article : Google Scholar | |
Ozga AJ, Chow MT and Luster AD: Chemokines and the immune response to cancer. Immunity. 54:859–874. 2021.PubMed/NCBI View Article : Google Scholar | |
Huang YC, Hou MF, Tsai YM, Pan YC, Tsai PH, Lin YS, Chang CY, Tsai EM and Hsu YL: Involvement of ACACA (acetyl-CoA carboxylase α) in the lung pre-metastatic niche formation in breast cancer by senescence phenotypic conversion in fibroblasts. Cell Oncol (Dordr). 46:643–660. 2023.PubMed/NCBI View Article : Google Scholar | |
Gu P, Sun M, Li L, Yang Y, Jiang Z, Ge Y, Wang W, Mu W and Wang H: Breast tumor-derived exosomal microRNA-200b-3p promotes specific organ metastasis through regulating CCL2 expression in lung epithelial cells. Front Cell Dev Biol. 9(657158)2021.PubMed/NCBI View Article : Google Scholar | |
Tanaka T, Kajiwara T, Torigoe T, Okamoto Y, Sato N and Tamura Y: Cancer-associated oxidoreductase ERO1-α drives the production of tumor-promoting myeloid-derived suppressor cells via oxidative protein folding. J Immunol. 194:2004–2010. 2015.PubMed/NCBI View Article : Google Scholar | |
Liu Y, Lai L, Chen Q, Song Y, Xu S, Ma F, Wang X, Wang J, Yu H, Cao X and Wang Q: MicroRNA-494 is required for the accumulation and functions of tumor-expanded myeloid-derived suppressor cells via targeting of PTEN. J Immunol. 188:5500–5510. 2012.PubMed/NCBI View Article : Google Scholar | |
Guo L, Kong D, Liu J, Zhan L, Luo L, Zheng W, Zheng Q, Chen C and Sun S: Breast cancer heterogeneity and its implication in personalized precision therapy. Exp Hematol Oncol. 12(3)2023.PubMed/NCBI View Article : Google Scholar | |
Vrakas CN, O'Sullivan RM, Evans SE, Ingram DA, Jones CB, Phuong T and Kurt RA: The Measure of DAMPs and a role for S100A8 in recruiting suppressor cells in breast cancer lung metastasis. Immunol Invest. 44:174–188. 2015.PubMed/NCBI View Article : Google Scholar | |
Chen JY, Lai YS, Chu PY, Chan SH, Wang LH and Hung WC: Cancer-derived VEGF-C increases chemokine production in lymphatic endothelial cells to promote CXCR2-dependent cancer invasion and MDSC recruitment. Cancers (Basel). 11(1120)2019.PubMed/NCBI View Article : Google Scholar | |
Roberts LM, Perez MJ, Balogh KN, Mingledorff G, Cross JV and Munson JM: Myeloid derived suppressor cells migrate in response to flow and lymphatic endothelial cell interaction in the breast tumor microenvironment. Cancers (Basel). 14(3008)2022.PubMed/NCBI View Article : Google Scholar | |
Yu B, Luo F, Sun B, Liu W, Shi Q, Cheng SY, Chen C, Chen G, Li Y and Feng H: KAT6A acetylation of SMAD3 regulates myeloid-derived suppressor cell recruitment, metastasis, and immunotherapy in triple-negative breast cancer. Adv Sci (Weinh). 8(e2100014)2021.PubMed/NCBI View Article : Google Scholar | |
Vadrevu SK, Chintala NK, Sharma SK, Sharma P, Cleveland C, Riediger L, Manne S, Fairlie DP, Gorczyca W, Almanza O, et al: Complement c5a receptor facilitates cancer metastasis by altering T-cell responses in the metastatic niche. Cancer Res. 74:3454–3465. 2014.PubMed/NCBI View Article : Google Scholar | |
Cheng R, Billet S, Liu C, Haldar S, Choudhury D, Tripathi M, Hav M, Merchant A, Hu T, Huang H, et al: Periodontal inflammation recruits distant metastatic breast cancer cells by increasing myeloid-derived suppressor cells. Oncogene. 39:1543–1556. 2020.PubMed/NCBI View Article : Google Scholar | |
Tcyganov E, Mastio J, Chen E and Gabrilovich DI: Plasticity of myeloid-derived suppressor cells in cancer. Curr Opin Immunol. 51:76–82. 2018.PubMed/NCBI View Article : Google Scholar | |
Mehta AK, Kadel S, Townsend MG, Oliwa M and Guerriero JL: Macrophage biology and mechanisms of immune suppression in breast cancer. Front Immunol. 12(643771)2021.PubMed/NCBI View Article : Google Scholar | |
Ostrand-Rosenberg S and Fenselau C: Myeloid-derived suppressor cells: immune-suppressive cells that impair antitumor immunity and are sculpted by their environment. J Immunol. 200:422–431. 2018.PubMed/NCBI View Article : Google Scholar | |
Cayrol C and Girard JP: Interleukin-33 (IL-33): A critical review of its biology and the mechanisms involved in its release as a potent extracellular cytokine. Cytokine. 156(155891)2022.PubMed/NCBI View Article : Google Scholar | |
Mattiola I and Diefenbach A: Enabling anti-tumor immunity by unleashing ILC2. Cell Res. 30:461–462. 2020.PubMed/NCBI View Article : Google Scholar | |
Halvorsen EC, Franks SE, Wadsworth BJ, Harbourne BT, Cederberg RA, Steer CA, Martinez-Gonzalez I, Calder J, Lockwood WW and Bennewith KL: IL-33 increases ST2+ Tregs and promotes metastatic tumour growth in the lungs in an amphiregulin-dependent manner. Oncoimmunology. 8(e1527497)2018.PubMed/NCBI View Article : Google Scholar | |
Gurram RK and Zhu J: Orchestration between ILC2s and Th2 cells in shaping type 2 immune responses. Cell Mol Immunol. 16:225–235. 2019.PubMed/NCBI View Article : Google Scholar | |
Choi MR, Sosman JA and Zhang B: The janus face of IL-33 signaling in tumor development and immune escape. Cancers (Basel). 13(3281)2021.PubMed/NCBI View Article : Google Scholar | |
Huang X, Cao J and Zu X: Tumor-associated macrophages: An important player in breast cancer progression. Thorac Cancer. 13:269–276. 2022.PubMed/NCBI View Article : Google Scholar | |
Hao NB, Lü MH, Fan YH, Cao YL, Zhang ZR and Yang SM: Macrophages in tumor microenvironments and the progression of tumors. Clin Dev Immunol. 2012(948098)2012.PubMed/NCBI View Article : Google Scholar | |
Boutilier AJ and Elsawa SF: Macrophage polarization states in the tumor microenvironment. Int J Mol Sci. 22(6995)2021.PubMed/NCBI View Article : Google Scholar | |
Wang S, Wang J, Chen Z, Luo J, Guo W, Sun L and Lin L: Targeting M2-like tumor-associated macrophages is a potential therapeutic approach to overcome antitumor drug resistance. NPJ Precis Oncol. 8(31)2024.PubMed/NCBI View Article : Google Scholar | |
Chen S, Saeed AFUH, Liu Q, Jiang Q, Xu H, Xiao GG, Rao L and Duo Y: Macrophages in immunoregulation and therapeutics. Signal Transduct Target Ther. 8(207)2023.PubMed/NCBI View Article : Google Scholar | |
Biswas S, Mandal G, Roy Chowdhury S, Purohit S, Payne KK, Anadon C, Gupta A, Swanson P, Yu X, Conejo-Garcia JR and Bhattacharyya A: Exosomes produced by mesenchymal stem cells drive differentiation of myeloid cells into immunosuppressive M2-polarized macrophages in breast cancer. J Immunol. 203:3447–3460. 2019.PubMed/NCBI View Article : Google Scholar | |
Payne KK, Zoon CK, Wan W, Marlar K, Keim RC, Kenari MN, Kazim AL, Bear HD and Manjili MH: Peripheral blood mononuclear cells of patients with breast cancer can be reprogrammed to enhance anti-HER-2/neu reactivity and overcome myeloid-derived suppressor cells. Breast Cancer Res Treat. 142:45–57. 2013.PubMed/NCBI View Article : Google Scholar | |
Gabrilovich DI, Ostrand-Rosenberg S and Bronte V: Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol. 12:253–268. 2012.PubMed/NCBI View Article : Google Scholar | |
Pansy K, Uhl B, Krstic J, Szmyra M, Fechter K, Santiso A, Thüminger L, Greinix H, Kargl J, Prochazka K, et al: Immune regulatory processes of the tumor microenvironment under malignant conditions. Int J Mol Sci. 22(13311)2021.PubMed/NCBI View Article : Google Scholar | |
Li F, Zhao Y, Wei L, Li S and Liu J: Tumor-infiltrating Treg, MDSC, and IDO expression associated with outcomes of neoadjuvant chemotherapy of breast cancer. Cancer Biol Ther. 19:695–705. 2018.PubMed/NCBI View Article : Google Scholar | |
Srivastava MK, Sinha P, Clements VK, Rodriguez P and Ostrand-Rosenberg S: Myeloid-derived suppressor cells inhibit T-cell activation by depleting cystine and cysteine. Cancer Res. 70:68–77. 2010.PubMed/NCBI View Article : Google Scholar | |
Lu T, Ramakrishnan R, Altiok S, Youn JI, Cheng P, Celis E, Pisarev V, Sherman S, Sporn MB and Gabrilovich D: Tumor-infiltrating myeloid cells induce tumor cell resistance to cytotoxic T cells in mice. J Clin Invest. 121:4015–4029. 2011.PubMed/NCBI View Article : Google Scholar | |
Stiff A, Trikha P, Mundy-Bosse B, McMichael E, Mace TA, Benner B, Kendra K, Campbell A, Gautam S and Abood D: , et al: Nitric oxide production by myeloid-derived suppressor cells plays a role in impairing Fc receptor-mediated natural killer cell function. Clin Cancer Res. 24:1891–1904. 2018.PubMed/NCBI View Article : Google Scholar | |
Sceneay J, Griessinger CM, Hoffmann SHL, Wen SW, Wong CSF, Krumeich S, Kneilling M, Pichler BJ and Möller A: Tracking the fate of adoptively transferred myeloid-derived suppressor cells in the primary breast tumor microenvironment. PLoS One. 13(e0196040)2018.PubMed/NCBI View Article : Google Scholar | |
Hanson EM, Clements VK, Sinha P, Ilkovitch D and Ostrand-Rosenberg S: Myeloid-derived suppressor cells down-regulate L-selectin expression on CD4+ and CD8+ T cells. J Immunol. 183:937–944. 2009.PubMed/NCBI View Article : Google Scholar | |
Sinha P, Chornoguz O, Clements VK, Artemenko KA, Zubarev RA and Ostrand-Rosenberg S: Myeloid-derived suppressor cells express the death receptor Fas and apoptose in response to T cell-expressed FasL. Blood. 117:5381–5390. 2011.PubMed/NCBI View Article : Google Scholar | |
Lelis FJ, Jaufmann J, Singh A, Fromm K, Teschner AC, Pöschel S, Schäfer I, Beer-Hammer S, Rieber N and Hartl D: Myeloid-derived suppressor cells modulate B-cell responses. Immunol Lett. 188:108–115. 2017.PubMed/NCBI View Article : Google Scholar | |
Shen M, Wang J, Yu W, Zhang C, Liu M, Wang K, Yang L, Wei F, Wang SE, Sun Q and Ren X: A novel MDSC-induced PD-1- PD-L1+ B-cell subset in breast tumor microenvironment possesses immuno-suppressive properties. Oncoimmunology. 7(e1413520)2018.PubMed/NCBI View Article : Google Scholar | |
Nam S, Lee A, Lim J and Lim JS: Analysis of the expression and regulation of PD-1 protein on the surface of myeloid-derived suppressor cells (MDSCs). Biomol Ther (Seoul). 27:63–70. 2019.PubMed/NCBI View Article : Google Scholar | |
Liu M, Wei F, Wang J, Yu W, Shen M, Liu T, Zhang D, Wang Y, Ren X and Sun Q: Myeloid-derived suppressor cells regulate the immunosuppressive functions of PD-1- PD-L1+ Bregs through PD-L1/PI3K/AKT/NF-κB axis in breast cancer. Cell Death Dis. 12(465)2021.PubMed/NCBI View Article : Google Scholar | |
Spallanzani RG, Dalotto-Moreno T, Raffo Iraolagoitia XL, Ziblat A, Domaica CI, Avila DE, Rossi LE, Fuertes MB, Battistone MA, Rabinovich GA, et al: Expansion of CD11b+ Ly6G+ Ly6C int cells driven by medroxyprogesterone acetate in mice bearing breast tumors restrains NK cell effector functions. Cancer Immunol Immunother. 62:1781–1795. 2013.PubMed/NCBI View Article : Google Scholar | |
Sceneay J, Chow MT, Chen A, Halse HM, Wong CS, Andrews DM, Sloan EK, Parker BS, Bowtell DD, Smyth MJ and Möller A: Primary tumor hypoxia recruits CD11b+/Ly6Cmed/Ly6G+ immune suppressor cells and compromises NK cell cytotoxicity in the premetastatic niche. Cancer Res. 72:3906–3911. 2012.PubMed/NCBI View Article : Google Scholar | |
Deng Z, Rong Y, Teng Y, Zhuang X, Samykutty A, Mu J, Zhang L, Cao P, Yan J, Miller D and Zhang HG: Exosomes miR-126a released from MDSC induced by DOX treatment promotes lung metastasis. Oncogene. 36:639–651. 2017.PubMed/NCBI View Article : Google Scholar | |
Ma X, Wang M, Yin T, Zhao Y and Wei X: Myeloid-derived suppressor cells promote metastasis in breast cancer after the stress of operative removal of the primary cancer. Front Oncol. 9(855)2019.PubMed/NCBI View Article : Google Scholar | |
Bergenfelz C, Roxå A, Mehmeti M, Leandersson K and Larsson AM: Clinical relevance of systemic monocytic-MDSCs in patients with metastatic breast cancer. Cancer Immunol Immunother. 69:435–448. 2020.PubMed/NCBI View Article : Google Scholar | |
Liu H, Wang Z, Zhou Y and Yang Y: MDSCs in breast cancer: An important enabler of tumor progression and an emerging therapeutic target. Front Immunol. 14(1199273)2023.PubMed/NCBI View Article : Google Scholar | |
Veglia F, Perego M and Gabrilovich D: Myeloid-derived suppressor cells coming of age. Nat Immunol. 19:108–119. 2018.PubMed/NCBI View Article : Google Scholar | |
Gatti-Mays ME, Balko JM, Gameiro SR, Bear HD, Prabhakaran S, Fukui J, Disis ML, Nanda R, Gulley JL, Kalinsky K, et al: If we build it they will come: targeting the immune response to breast cancer. NPJ Breast Cancer. 5(37)2019.PubMed/NCBI View Article : Google Scholar | |
Kim K, Skora AD, Li Z, Liu Q, Tam AJ, Blosser RL, Diaz LA Jr, Papadopoulos N, Kinzler KW, Vogelstein B and Zhou S: Eradication of metastatic mouse cancers resistant to immune checkpoint blockade by suppression of myeloid-derived cells. Proc Natl Acad Sci USA. 111:11774–11779. 2014.PubMed/NCBI View Article : Google Scholar | |
Le HK, Graham L, Cha E, Morales JK, Manjili MH and Bear HD: Gemcitabine directly inhibits myeloid derived suppressor cells in BALB/c mice bearing 4T1 mammary carcinoma and augments expansion of T cells from tumor-bearing mice. Int Immunopharmacol. 9:900–909. 2009.PubMed/NCBI View Article : Google Scholar | |
Alizadeh D, Trad M, Hanke NT, Larmonier CB, Janikashvili N, Bonnotte B, Katsanis E and Larmonier N: Doxorubicin eliminates myeloid-derived suppressor cells and enhances the efficacy of adoptive T-cell transfer in breast cancer. Cancer Res. 74:104–118. 2014.PubMed/NCBI View Article : Google Scholar | |
Vincent J, Mignot G, Chalmin F, Ladoire S, Bruchard M, Chevriaux A, Martin F, Apetoh L, Rébé C and Ghiringhelli F: 5-Fluorouracil selectively kills tumor-associated myeloid-derived suppressor cells resulting in enhanced T cell-dependent antitumor immunity. Cancer Res. 70:3052–3061. 2010.PubMed/NCBI View Article : Google Scholar | |
Sharma P, Abramson V, O’Dea A, Nye L, Mayer I, Crane G, Elia M, Yoder R, Staley J, Schwensen K, et al: Romidepsin (HDACi) plus cisplatin and nivolumab triplet combination in patients with metastatic triple negative breast cancer (mTNBC). J Clin Oncol. 39(10.1200/JCO.2021.39.15_suppl.1076)2021. | |
Davis RJ, Moore EC, Clavijo PE, Friedman J, Cash H, Chen Z, Silvin C, Van Waes C and Allen C: Anti-PD-L1 efficacy can be enhanced by inhibition of myeloid-derived suppressor cells with a selective inhibitor of PI3Kδ/γ. Cancer Res. 77:2607–2619. 2017.PubMed/NCBI View Article : Google Scholar | |
Tu SP, Jin H, Shi JD, Zhu LM, Suo Y, Lu G, Liu A, Wang TC and Yang CS: Curcumin induces the differentiation of myeloid-derived suppressor cells and inhibits their interaction with cancer cells and related tumor growth. Cancer Prev Res (Phila). 5:205–215. 2012.PubMed/NCBI View Article : Google Scholar | |
Sánchez-León ML, Jiménez-Cortegana C, Silva Romeiro S, Garnacho C, de la Cruz-Merino L, García-Domínguez DJ, Hontecillas-Prieto L and Sánchez-Margalet V: Defining the emergence of new immunotherapy approaches in breast cancer: Role of myeloid-derived suppressor cells. Int J Mol Sci. 24(5208)2023.PubMed/NCBI View Article : Google Scholar | |
Kusmartsev S, Cheng F, Yu B, Nefedova Y, Sotomayor E, Lush R and Gabrilovich D: All-trans-retinoic acid eliminates immature myeloid cells from tumor-bearing mice and improves the effect of vaccination. Cancer Res. 63:4441–4449. 2003.PubMed/NCBI | |
Iclozan C, Antonia S, Chiappori A, Chen DT and Gabrilovich D: Therapeutic regulation of myeloid-derived suppressor cells and immune response to cancer vaccine in patients with extensive stage small cell lung cancer. Cancer Immunol Immunother. 62:909–918. 2013.PubMed/NCBI View Article : Google Scholar | |
Forghani P, Khorramizadeh MR and Waller EK: Silibinin inhibits accumulation of myeloid-derived suppressor cells and tumor growth of murine breast cancer. Cancer Med. 3:215–224. 2014.PubMed/NCBI View Article : Google Scholar | |
Sawant A, Deshane J, Jules J, Lee CM, Harris BA, Feng X and Ponnazhagan S: Myeloid-derived suppressor cells function as novel osteoclast progenitors enhancing bone loss in breast cancer. Cancer Res. 73:672–682. 2013.PubMed/NCBI View Article : Google Scholar | |
Kugler A, Stuhler G, Walden P, Zöller G, Zobywalski A, Brossart P, Trefzer U, Ullrich S, Müller CA, Becker V, et al: Regression of human metastatic renal cell carcinoma after vaccination with tumor cell-dendritic cell hybrids. Nat Med. 6:332–336. 2000.PubMed/NCBI View Article : Google Scholar | |
Thakur A, Schalk D, Sarkar SH, Al-Khadimi Z, Sarkar FH and Lum LG: A Th1 cytokine-enriched microenvironment enhances tumor killing by activated T cells armed with bispecific antibodies and inhibits the development of myeloid-derived suppressor cells. Cancer Immunol Immunother. 61:497–509. 2012.PubMed/NCBI View Article : Google Scholar | |
Kmieciak M, Basu D, Payne KK, Toor A, Yacoub A, Wang XY, Smith L, Bear HD and Manjili MH: Activated NK T cells and NK cells render T cells resistant to MDSC and result in an effective adoptive cellular therapy against breast cancer in the FVBN202 transgenic mouse. J Immunol. 187:708–717. 2011.PubMed/NCBI View Article : Google Scholar | |
Chandra D, Jahangir A, Quispe-Tintaya W, Einstein MH and Gravekamp C: Myeloid-derived suppressor cells have a central role in attenuated Listeria monocytogenes-based immunotherapy against metastatic breast cancer in young and old mice. Br J Cancer. 108:2281–2290. 2013.PubMed/NCBI View Article : Google Scholar | |
Chaves NL, Amorim DA, Lopes CAP, Estrela-Lopis I, Böttner J, de Souza AR and Báo SN: Comparison of the effect of rhodium citrate-associated iron oxide nanoparticles on metastatic and non-metastatic breast cancer cells. Cancer Nano. 10:1–12. 2019. | |
Yao Y, Zhou Y, Liu L, Xu Y, Chen Q, Wang Y, Wu S, Deng Y, Zhang J and Shao A: Nanoparticle-based drug delivery in cancer therapy and its role in overcoming drug resistance. Front Mol Biosci. 7(193)2020.PubMed/NCBI View Article : Google Scholar | |
Chaves NL, Estrela-Lopis I, Böttner J, Lopes CA, Guido BC, de Sousa AR and Báo SN: Exploring cellular uptake of iron oxide nanoparticles associated with rhodium citrate in breast cancer cells. Int J Nanomedicine. 12:5511–5523. 2017.PubMed/NCBI View Article : Google Scholar | |
Figueiro Longo JP and Muehlmann LA: Nanomedicine beyond tumor passive targeting: What next? Nanomedicine (Lond). 15:1819–1822. 2020.PubMed/NCBI View Article : Google Scholar | |
Zhang N, Liu S, Shi S, Chen Y, Xu F, Wei X and Xu Y: Solubilization and delivery of Ursolic-acid for modulating tumor microenvironment and regulatory T cell activities in cancer immunotherapy. J Control Release. 320:168–178. 2020.PubMed/NCBI View Article : Google Scholar | |
Chen C, Li A, Sun P, Xu J, Du W, Zhang J, Liu Y, Zhang R, Zhang S, Yang Z, et al: Efficiently restoring the tumoricidal immunity against resistant malignancies via an immune nanomodulator. J Control Release. 324:574–585. 2020.PubMed/NCBI View Article : Google Scholar | |
Ali R, Shao H and Varamini P: Potential Nanotechnology-Based Therapeutics to Prevent Cancer Progression through TME Cell-Driven Populations. Pharmaceutics. 15(112)2022.PubMed/NCBI View Article : Google Scholar | |
Lu Z, Liu H, Ma L, Ren K, He Z, Li M and He Q: Micellar nanoparticles inhibit breast cancer and pulmonary metastasis by modulating the recruitment and depletion of myeloid-derived suppressor cells. Nanoscale. 14:17315–17330. 2022.PubMed/NCBI View Article : Google Scholar | |
Debien V, De Caluwé A, Wang X, Piccart-Gebhart M, Tuohy VK, Romano E and Buisseret L: Immunotherapy in breast cancer: An overview of current strategies and perspectives. NPJ Breast Cancer. 9(7)2023.PubMed/NCBI View Article : Google Scholar | |
Teschendorff AE, Miremadi A, Pinder SE, Ellis IO and Caldas C: An immune response gene expression module identifies a good prognosis subtype in estrogen receptor negative breast cancer. Genome Biol. 8(R157)2007.PubMed/NCBI View Article : Google Scholar |