Immature myeloid-derived suppressor cells: A bridge between inflammation and cancer (Review)
- Authors:
- Caterina Musolino
- Alessandro Allegra
- Govanni Pioggia
- Sebastiano Gangemi
-
Affiliations: Division of Hematology, Department of General Surgery, Pathological Anatomy and Oncology, University of Messina, Messina, Italy, Institute of Clinical Physiology, IFN CNR, Messina Unit, Messina, Italy, School and Division of Allergy and Clinical Immunology, Department of Clinical and Experimental Medicine, University Hospital ʻG. Martinoʼ, Messina, Italy - Published online on: December 5, 2016 https://doi.org/10.3892/or.2016.5291
- Pages: 671-683
This article is mentioned in:
Abstract
Balkwill F and Mantovani A: Inflammation and cancer: back to Virchow? Lancet. 357:539–545. 2001. View Article : Google Scholar : PubMed/NCBI | |
Kuper H, Adami HO and Trichopoulos D: Infections as a major preventable cause of human cancer. J Intern Med. 248:171–183. 2000. View Article : Google Scholar : PubMed/NCBI | |
Shacter E and Weitzman SA: Chronic inflammation and cancer. Oncology (Williston Park). 16:217–232. 2002.PubMed/NCBI | |
Coussens LM and Werb Z: Inflammation and cancer. Nature. 420:860–867. 2002. View Article : Google Scholar : PubMed/NCBI | |
Kusmartsev S and Gabrilovich DI: Immature myeloid cells and cancer-associated immune suppression. Cancer Immunol Immunother. 51:293–298. 2002. View Article : Google Scholar : PubMed/NCBI | |
Serafini P, De Santo C, Marigo I, Cingarlini S, Dolcetti L, Gallina G, Zanovello P and Bronte V: Derangement of immune responses by myeloid suppressor cells. Cancer Immunol Immunother. 53:64–72. 2004. View Article : Google Scholar : PubMed/NCBI | |
Vakkila J and Lotze MT: Inflammation and necrosis promote tumour growth. Nat Rev Immunol. 4:641–648. 2004. View Article : Google Scholar : PubMed/NCBI | |
Aller MA, Arias JL, Nava MP and Arias J: Posttraumatic inflammation is a complex response based on the pathological expression of the nervous, immune, and endocrine functional systems. Exp Biol Med. 229:170–181. 2004. View Article : Google Scholar | |
Denko NC, Fontana LA, Hudson KM, Sutphin PD, Raychaudhuri S, Altman R and Giaccia AJ: Investigating hypoxic tumor physiology through gene expression patterns. Oncogene. 22:5907–5914. 2003. View Article : Google Scholar : PubMed/NCBI | |
Whiteside TL: The tumor microenvironment and its role in promoting tumor growth. Oncogene. 27:5904–5912. 2008. View Article : Google Scholar : PubMed/NCBI | |
Srivastava MK, Andersson Å, Zhu L, Harris-White M, Lee JM, Dubinett S and Sharma S: Myeloid suppressor cells and immune modulation in lung cancer. Immunotherapy. 4:291–304. 2012. View Article : Google Scholar : PubMed/NCBI | |
Gallucci S and Matzinger P: Danger signals: SOS to the immune system. Curr Opin Immunol. 13:114–119. 2001. View Article : Google Scholar : PubMed/NCBI | |
Whiteside TL: Immune suppression in cancer: effects on immune cells, mechanisms and future therapeutic intervention. Semin Cancer Biol. 16:3–15. 2006. View Article : Google Scholar : PubMed/NCBI | |
Smyth MJ, Dunn GP and Schreiber RD: Cancer immunosurveillance and immunoediting: The roles of immunity in suppressing tumor development and shaping tumor immunogenicity. Adv Immunol. 90:1–50. 2006. View Article : Google Scholar : PubMed/NCBI | |
Poggi A and Zocchi MR: Mechanisms of tumor escape: role of tumor microenvironment in inducing apoptosis of cytolytic effector cells. Arch Immunol Ther Exp. 54:323–333. 2006. View Article : Google Scholar | |
Strober S: Natural suppressor (NS) cells, neonatal tolerance, and total lymphoid irradiation: exploring obscure relationships. Annu Rev Immunol. 2:219–237. 1984. View Article : Google Scholar : PubMed/NCBI | |
Gabrilovich DI, Velders MP, Sotomayor EM and Kast WM: Mechanism of immune dysfunction in cancer mediated by immature Gr-1+ myeloid cells. J Immunol. 166:5398–5406. 2001. View Article : Google Scholar : PubMed/NCBI | |
Bronte V, Serafini P, De Santo C, Marigo I, Tosello V, Mazzoni A, Segal DM, Staib C, Lowel M, Sutter G, et al: IL-4-induced arginase 1 suppresses alloreactive T cells in tumor-bearing mice. J Immunol. 170:270–278. 2003. View Article : Google Scholar : PubMed/NCBI | |
Liu Y, Van Ginderachter JA, Brys L, De Baetselier P, Raes G and Geldhof AB: Nitric oxide-independent CTL suppression during tumor progression: association with arginase-producing (M2) myeloid cells. J Immunol. 170:5064–5074. 2003. View Article : Google Scholar : PubMed/NCBI | |
Mazzoni A, Bronte V, Visintin A, Spitzer JH, Apolloni E, Serafini P, Zanovello P and Segal DM: Myeloid suppressor lines inhibit T cell responses by an NO-dependent mechanism. J Immunol. 168:689–695. 2002. View Article : Google Scholar : PubMed/NCBI | |
Rodriguez PC, Quiceno DG, Zabaleta J, Ortiz B, Zea AH, Piazuelo MB, Delgado A, Correa P, Brayer J, Sotomayor EM, et al: Arginase I production in the tumor microenvironment by mature myeloid cells inhibits T-cell receptor expression and antigen-specific T-cell responses. Cancer Res. 64:5839–5849. 2004. View Article : Google Scholar : PubMed/NCBI | |
Bronte V, Apolloni E, Cabrelle A, Ronca R, Serafini P, Zamboni P, Restifo NP and Zanovello P: Identification of a CD11b(+)/Gr-1(+)/CD31(+) myeloid progenitor capable of activating or suppressing CD8(+) T cells. Blood. 96:3838–3846. 2000.PubMed/NCBI | |
Kusmartsev S and Gabrilovich DI: Inhibition of myeloid cell differentiation in cancer: the role of reactive oxygen species. J Leukoc Biol. 74:186–196. 2003. View Article : Google Scholar : PubMed/NCBI | |
Li Q, Pan PY, Gu P, Xu D and Chen SH: Role of immature myeloid Gr-1+ cells in the development of antitumor immunity. Cancer Res. 64:1130–1139. 2004. View Article : Google Scholar : PubMed/NCBI | |
Gabrilovich DI: Molecular mechanisms and therapeutic reversal of immune suppression in cancer. Curr Cancer Drug Targets. 7:12007. View Article : Google Scholar : PubMed/NCBI | |
Youn JI, Nagaraj S, Collazo M and Gabrilovich DI: Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J Immunol. 181:5791–5802. 2008. View Article : Google Scholar : PubMed/NCBI | |
Youn JI and Gabrilovich DI: The biology of myeloid-derived suppressor cells: the blessing and the curse of morphological and functional heterogeneity. Eur J Immunol. 40:2969–2975. 2010. View Article : Google Scholar : PubMed/NCBI | |
Condamine T and Gabrilovich DI: Molecular mechanisms regulating myeloid-derived suppressor cell differentiation and function. Trends Immunol. 32:19–25. 2011. View Article : Google Scholar : PubMed/NCBI | |
Zea AH, Rodriguez PC, Atkins MB, Hernandez C, Signoretti S, Zabaleta J, McDermott D, Quiceno D, Youmans A, O'Neill A, et al: Arginase-producing myeloid suppressor cells in renal cell carcinoma patients: a mechanism of tumor evasion. Cancer Res. 65:3044–3048. 2005.PubMed/NCBI | |
Poschke I, Mougiakakos D, Hansson J, Masucci GV and Kiessling R: Immature immunosuppressive CD14+HLA-DR-/low cells in melanoma patients are Stat3hi and overexpress CD80, CD83, and DC-Sign. Cancer Res. 70:4335–4345. 2010. View Article : Google Scholar : PubMed/NCBI | |
Srivastava MK, Bosch JJ, Thompson JA, Ksander BR, Edelman MJ and Ostrand-Rosenberg S: Lung cancer patients' CD4(+) T cells are activated in vitro by MHC II cell-based vaccines despite the presence of myeloid-derived suppressor cells. Cancer Immunol Immunother. 57:1493–1504. 2008. View Article : Google Scholar : PubMed/NCBI | |
Almand B, Clark JI, Nikitina E, van Beynen J, English NR, Knight SC, Carbone DP and Gabrilovich DI: Increased production of immature myeloid cells in cancer patients: a mechanism of immunosuppression in cancer. J Immunol. 166:678–689. 2001. View Article : Google Scholar : PubMed/NCBI | |
Peláez B, Campillo JA, López-Asenjo JA and Subiza JL: Cyclophosphamide induces the development of early myeloid cells suppressing tumor cell growth by a nitric oxide-dependent mechanism. J Immunol. 166:6608–6615. 2001. View Article : Google Scholar : PubMed/NCBI | |
Goddard S, Youster J, Morgan E and Adams DH: Interleukin-10 secretion differentiates dendritic cells from human liver and skin. Am J Pathol. 164:511–519. 2004. View Article : Google Scholar : PubMed/NCBI | |
Halliday GM and Le S: Transforming growth factor-β produced by progressor tumors inhibits, while IL-10 produced by regressor tumors enhances, Langerhans cell migration from skin. Int Immunol. 13:1147–1154. 2001. View Article : Google Scholar : PubMed/NCBI | |
Chomarat P, Banchereau J, Davoust J and Palucka AK: IL-6 switches the differentiation of monocytes from dendritic cells to macrophages. Nat Immunol. 1:510–514. 2000. View Article : Google Scholar : PubMed/NCBI | |
Gabrilovich DI, Chen HL, Girgis KR, Cunningham HT, Meny GM, Nadaf S, Kavanaugh D and Carbone DP: Production of vascular endothelial growth factor by human tumors inhibits the functional maturation of dendritic cells. Nat Med. 2:1096–1103. 1996. View Article : Google Scholar : PubMed/NCBI | |
Hammad H, de Heer HJ, Soullie T, Hoogsteden HC, Trottein F and Lambrecht BN: Prostaglandin D2 inhibits airway dendritic cell migration and function in steady state conditions by selective activation of the D prostanoid receptor 1. J Immunol. 171:3936–3940. 2003. View Article : Google Scholar : PubMed/NCBI | |
Jing H, Vassiliou E and Ganea D: Prostaglandin E2 inhibits production of the inflammatory chemokines CCL3 and CCL4 in dendritic cells. J Leukoc Biol. 74:868–879. 2003. View Article : Google Scholar : PubMed/NCBI | |
Schnurr M, Toy T, Shin A, Hartmann G, Rothenfusser S, Soellner J, Davis ID, Cebon J and Maraskovsky E: Role of adenosine receptors in regulating chemotaxis and cytokine production of plasmacytoid dendritic cells. Blood. 103:1391–1397. 2004. View Article : Google Scholar : PubMed/NCBI | |
Murdoch C, Muthana M, Coffelt SB and Lewis CE: The role of myeloid cells in the promotion of tumour angiogenesis. Nat Rev Cancer. 8:618–631. 2008. View Article : Google Scholar : PubMed/NCBI | |
Sica A and Bronte V: Altered macrophage differentiation and immune dysfunction in tumor development. J Clin Invest. 117:1155–1166. 2007. View Article : Google Scholar : PubMed/NCBI | |
Bunt SK, Yang L, Sinha P, Clements VK, Leips J and Ostrand-Rosenberg S: Reduced inflammation in the tumor microenvironment delays the accumulation of myeloid-derived suppressor cells and limits tumor progression. Cancer Res. 67:10019–10026. 2007. View Article : Google Scholar : PubMed/NCBI | |
Bunt SK, Sinha P, Clements VK, Leips J and Ostrand-Rosenberg S: Inflammation induces myeloid-derived suppressor cells that facilitate tumor progression. J Immunol. 176:284–290. 2006. View Article : Google Scholar : PubMed/NCBI | |
Jiang H, Gebhardt C, Umansky L, Beckhove P, Schulze TJ, Utikal J and Umansky V: Elevated chronic inflammatory factors and myeloid-derived suppressor cells indicate poor prognosis in advanced melanoma patients. Int J Cancer. 136:2352–2360. 2015. View Article : Google Scholar : PubMed/NCBI | |
Blaser MJ, Chyou PH and Nomura A: Age at establishment of Helicobacter pylori infection and gastric carcinoma, gastric ulcer, and duodenal ulcer risk. Cancer Res. 55:562–565. 1995.PubMed/NCBI | |
Ernst PB and Gold BD: The disease spectrum of Helicobacter pylori: the immunopathogenesis of gastroduodenal ulcer and gastric cancer. Annu Rev Microbiol. 54:615–640. 2000. View Article : Google Scholar : PubMed/NCBI | |
Kohanbash G, McKaveney K, Sakaki M, Ueda R, Mintz AH, Amankulor N, Fujita M, Ohlfest JR and Okada H: GM-CSF promotes the immunosuppressive activity of glioma-infiltrating myeloid cells through interleukin-4 receptor-α. Cancer Res. 73:6413–6423. 2013. View Article : Google Scholar : PubMed/NCBI | |
Sade-Feldman M, Kanterman J, Ish-Shalom E, Elnekave M, Horwitz E and Baniyash M: Tumor necrosis factor-α blocks differentiation and enhances suppressive activity of immature myeloid cells during chronic inflammation. Immunity. 38:541–554. 2013. View Article : Google Scholar : PubMed/NCBI | |
Polz J, Remke A, Weber S, Schmidt D, Weber-Steffens D, Pietryga-Krieger A, Müller N, Ritter U, Mostböck S and Männel DN: Myeloid suppressor cells require membrane TNFR2 expression for suppressive activity. Immun Inflamm Dis. 2:121–130. 2014. View Article : Google Scholar : PubMed/NCBI | |
Sinha P, Okoro C, Foell D, Freeze HH, Ostrand-Rosenberg S and Srikrishna G: Proinflammatory S100 proteins regulate the accumulation of myeloid-derived suppressor cells. J Immunol. 181:4666–4675. 2008. View Article : Google Scholar : PubMed/NCBI | |
Cheng P, Corzo CA, Luetteke N, Yu B, Nagaraj S, Bui MM, Ortiz M, Nacken W, Sorg C, Vogl T, et al: Inhibition of dendritic cell differentiation and accumulation of myeloid-derived suppressor cells in cancer is regulated by S100A9 protein. J Exp Med. 205:2235–2249. 2008. View Article : Google Scholar : PubMed/NCBI | |
Tsan MF: Toll-like receptors, inflammation and cancer. Semin Cancer Biol. 16:32–37. 2006. View Article : Google Scholar : PubMed/NCBI | |
Vaknin I, Blinder L, Wang L, Gazit R, Shapira E, Genina O, Pines M, Pikarsky E and Baniyash M: A common pathway mediated through Toll-like receptors leads to T- and natural killer-cell immunosuppression. Blood. 111:1437–1447. 2008. View Article : Google Scholar : PubMed/NCBI | |
Nakagomi H, Petersson M, Magnusson I, Juhlin C, Matsuda M, Mellstedt H, Taupin JL, Vivier E, Anderson P and Kiessling R: Decreased expression of the signal-transducing ζ chains in tumor-infiltrating T-cells and NK cells of patients with colorectal carcinoma. Cancer Res. 53:5610–5612. 1993.PubMed/NCBI | |
Matsuda M, Petersson M, Lenkei R, Taupin JL, Magnusson I, Mellstedt H, Anderson P and Kiessling R: Alterations in the signal-transducing molecules of T cells and NK cells in colorectal tumor-infiltrating, gut mucosal and peripheral lymphocytes: correlation with the stage of the disease. Int J Cancer. 61:765–772. 1995. View Article : Google Scholar : PubMed/NCBI | |
Lai P, Rabinowich H, Crowley-Nowick PA, Bell MC, Mantovani G and Whiteside TL: Alterations in expression and function of signal-transducing proteins in tumor-associated T and natural killer cells in patients with ovarian carcinoma. Clin Cancer Res. 2:161–173. 1996.PubMed/NCBI | |
Kono K, Ressing ME, Brandt RM, Melief CJ, Potkul RK, Andersson B, Petersson M, Kast WM and Kiessling R: Decreased expression of signal-transducing ζ chain in peripheral T cells and natural killer cells in patients with cervical cancer. Clin Cancer Res. 2:1825–1828. 1996.PubMed/NCBI | |
Kurt RA, Urba WJ, Smith JW and Schoof DD: Peripheral T lymphocytes from women with breast cancer exhibit abnormal protein expression of several signaling molecules. Int J Cancer. 78:16–20. 1998. View Article : Google Scholar : PubMed/NCBI | |
Kuss I, Saito T, Johnson JT and Whiteside TL: Clinical significance of decreased ζ chain expression in peripheral blood lymphocytes of patients with head and neck cancer. Clin Cancer Res. 5:329–334. 1999.PubMed/NCBI | |
Healy CG, Simons JW, Carducci MA, DeWeese TL, Bartkowski M, Tong KP and Bolton WE: Impaired expression and function of signal-transducing ζ chains in peripheral T cells and natural killer cells in patients with prostate cancer. Cytometry. 32:109–119. 1998. View Article : Google Scholar : PubMed/NCBI | |
Ezernitchi AV, Vaknin I, Cohen-Daniel L, Levy O, Manaster E, Halabi A, Pikarsky E, Shapira L and Baniyash M: TCR ζ downregulation under chronic inflammation is mediated by myeloid suppressor cells differentially distributed between various lymphatic organs. J Immunol. 177:4763–4772. 2006. View Article : Google Scholar : PubMed/NCBI | |
Baniyash M: TCR ζ-chain downregulation: curtailing an excessive inflammatory immune response. Nat Rev Immunol. 4:675–687. 2004. View Article : Google Scholar : PubMed/NCBI | |
Baniyash M: Chronic inflammation, immunosuppression and cancer: new insights and outlook. Semin Cancer Biol. 16:80–88. 2006. View Article : Google Scholar : PubMed/NCBI | |
Gabrilovich D, Ishida T, Oyama T, Ran S, Kravtsov V, Nadaf S and Carbone DP: Vascular endothelial growth factor inhibits the development of dendritic cells and dramatically affects the differentiation of multiple hematopoietic lineages in vivo. Blood. 92:4150–4166. 1998.PubMed/NCBI | |
Wang T, Niu G, Kortylewski M, Burdelya L, Shain K, Zhang S, Bhattacharya R, Gabrilovich D, Heller R, Coppola D, et al: Regulation of the innate and adaptive immune responses by Stat-3 signaling in tumor cells. Nat Med. 10:48–54. 2004. View Article : Google Scholar : PubMed/NCBI | |
Marigo I, Dolcetti L, Serafini P, Zanovello P and Bronte V: Tumor-induced tolerance and immune suppression by myeloid derived suppressor cells. Immunol Rev. 222:162–179. 2008. View Article : Google Scholar : PubMed/NCBI | |
Serafini P, Borrello I and Bronte V: Myeloid suppressor cells in cancer: recruitment, phenotype, properties, and mechanisms of immune suppression. Semin Cancer Biol. 16:53–65. 2006. View Article : Google Scholar : PubMed/NCBI | |
Bronte V, Chappell DB, Apolloni E, Cabrelle A, Wang M, Hwu P and Restifo NP: Unopposed production of granulocyte-macrophage colony-stimulating factor by tumors inhibits CD8+ T cell responses by dysregulating antigen-presenting cell maturation. J Immunol. 162:5728–5737. 1999.PubMed/NCBI | |
Serafini P, Carbley R, Noonan KA, Tan G, Bronte V and Borrello I: High-dose granulocyte-macrophage colony-stimulating factor-producing vaccines impair the immune response through the recruitment of myeloid suppressor cells. Cancer Res. 64:6337–6343. 2004. View Article : Google Scholar : PubMed/NCBI | |
Fujita M, Kohanbash G, Fellows-Mayle W, Hamilton RL, Komohara Y, Decker SA, Ohlfest JR and Okada H: COX-2 blockade suppresses gliomagenesis by inhibiting myeloid-derived suppressor cells. Cancer Res. 71:2664–2674. 2011. View Article : Google Scholar : PubMed/NCBI | |
Mundy-Bosse BL, Lesinski GB, Jaime-Ramirez AC, Benninger K, Khan M, Kuppusamy P, Guenterberg K, Kondadasula SV, Chaudhury AR, La Perle KM, et al: Myeloid-derived suppressor cell inhibition of the IFN response in tumor-bearing mice. Cancer Res. 71:5101–5110. 2011. View Article : Google Scholar : PubMed/NCBI | |
McKenna KC, Beatty KM, Bilonick RA, Schoenfield L, Lathrop KL and Singh AD: Activated CD11b+CD15+ granulocytes increase in the blood of patients with uveal melanoma. Invest Ophthalmol Vis Sci. 50:4295–4303. 2009. View Article : Google Scholar : PubMed/NCBI | |
Young MR, Petruzzelli GJ, Kolesiak K, Achille N, Lathers DM and Gabrilovich DI: Human squamous cell carcinomas of the head and neck chemoattract immune suppressive CD34(+) progenitor cells. Hum Immunol. 62:332–341. 2001. View Article : Google Scholar : PubMed/NCBI | |
Filipazzi P, Valenti R, Huber V, Pilla L, Canese P, Iero M, Castelli C, Mariani L, Parmiani G and Rivoltini L: Identification of a new subset of myeloid suppressor cells in peripheral blood of melanoma patients with modulation by a granulocyte-macrophage colony-stimulation factor-based antitumor vaccine. J Clin Oncol. 25:2546–2553. 2007. View Article : Google Scholar : PubMed/NCBI | |
Achberger S, Aldrich W, Tubbs R, Crabb JW, Singh AD and Triozzi PL: Circulating immune cell and microRNA in patients with uveal melanoma developing metastatic disease. Mol Immunol. 58:182–186. 2014. View Article : Google Scholar : PubMed/NCBI | |
Danna EA, Sinha P, Gilbert M, Clements VK, Pulaski BA and Ostrand-Rosenberg S: Surgical removal of primary tumor reverses tumor-induced immunosuppression despite the presence of metastatic disease. Cancer Res. 64:2205–2211. 2004. View Article : Google Scholar : PubMed/NCBI | |
Sinha P, Clements VK and Ostrand-Rosenberg S: Reduction of myeloid-derived suppressor cells and induction of M1 macrophages facilitate the rejection of established metastatic disease. J Immunol. 174:636–645. 2005. View Article : Google Scholar : PubMed/NCBI | |
Almand B, Resser JR, Lindman B, Nadaf S, Clark JI, Kwon ED, Carbone DP and Gabrilovich DI: Clinical significance of defective dendritic cell differentiation in cancer. Clin Cancer Res. 6:1755–1766. 2000.PubMed/NCBI | |
Tinder TL, Subramani DB, Basu GD, Bradley JM, Schettini J, Million A, Skaar T and Mukherjee P: MUC1 enhances tumor progression and contributes toward immunosuppression in a mouse model of spontaneous pancreatic adenocarcinoma. J Immunol. 181:3116–3125. 2008. View Article : Google Scholar : PubMed/NCBI | |
Wolf AM, Wolf D, Steurer M, Gastl G, Gunsilius E and Grubeck-Loebenstein B: Increase of regulatory T cells in the peripheral blood of cancer patients. Clin Cancer Res. 9:606–612. 2003.PubMed/NCBI | |
Terabe M and Berzofsky JA: Immunoregulatory T cells in tumor immunity. Curr Opin Immunol. 16:157–162. 2004. View Article : Google Scholar : PubMed/NCBI | |
Cuenca A, Cheng F, Wang H, Brayer J, Horna P, Gu L, Bien H, Borrello IM, Levitsky HI and Sotomayor EM: Extra-lymphatic solid tumor growth is not immunologically ignored and results in early induction of antigen-specific T-cell anergy: dominant role of cross-tolerance to tumor antigens. Cancer Res. 63:9007–9015. 2003.PubMed/NCBI | |
Schmidt-Wolf IG, Dejbakhsh-Jones S, Ginzton N, Greenberg P and Strober S: T-cell subsets and suppressor cells in human bone marrow. Blood. 80:3242–3250. 1992.PubMed/NCBI | |
Young MR, Wright MA, Matthews JP, Malik I and Prechel M: Suppression of T cell proliferation by tumor-induced granulocyte-macrophage progenitor cells producing transforming growth factor-β and nitric oxide. J Immunol. 156:1916–1922. 1996.PubMed/NCBI | |
Angulo I, Rodríguez R, García B, Medina M, Navarro J and Subiza JL: Involvement of nitric oxide in bone marrow-derived natural suppressor activity. Its dependence on IFN-γ. J Immunol. 155:15–26. 1995.PubMed/NCBI | |
Brooks JC and Hoskin DW: The inhibitory effect of cyclophosphamide-induced MAC-1+ natural suppressor cells on IL-2 and IL-4 utilization in MLR. Transplantation. 58:1096–1103. 1994. View Article : Google Scholar : PubMed/NCBI | |
Kusmartsev SA, Li Y and Chen SH: Gr-1+ myeloid cells derived from tumor-bearing mice inhibit primary T cell activation induced through CD3/CD28 costimulation. J Immunol. 165:779–785. 2000. View Article : Google Scholar : PubMed/NCBI | |
Rodriguez PC, Zea AH, DeSalvo J, Culotta KS, Zabaleta J, Quiceno DG, Ochoa JB and Ochoa AC: L-arginine consumption by macrophages modulates the expression of CD3 ζ chain in T lymphocytes. J Immunol. 171:1232–1239. 2003. View Article : Google Scholar : PubMed/NCBI | |
Bronte V, Serafini P, Mazzoni A, Segal DM and Zanovello P: L-arginine metabolism in myeloid cells controls T-lymphocyte functions. Trends Immunol. 24:302–306. 2003. View Article : Google Scholar : PubMed/NCBI | |
Kusmartsev S, Nefedova Y, Yoder D and Gabrilovich DI: Antigen-specific inhibition of CD8+ T cell response by immature myeloid cells in cancer is mediated by reactive oxygen species. J Immunol. 172:989–999. 2004. View Article : Google Scholar : PubMed/NCBI | |
Schmielau J and Finn OJ: Activated granulocytes and granulocyte-derived hydrogen peroxide are the underlying mechanism of suppression of T-cell function in advanced cancer patients. Cancer Res. 61:4756–4760. 2001.PubMed/NCBI | |
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. View Article : Google Scholar : PubMed/NCBI | |
Li H, Han Y, Guo Q, Zhang M and Cao X: Cancer-expanded myeloid-derived suppressor cells induce anergy of NK cells through membrane-bound TGF-β 1. J Immunol. 182:240–249. 2009. View Article : Google Scholar : PubMed/NCBI | |
Rodriguez PC, Hernandez CP, Quiceno D, Dubinett SM, Zabaleta J, Ochoa JB, Gilbert J and Ochoa AC: Arginase I in myeloid suppressor cells is induced by COX-2 in lung carcinoma. J Exp Med. 202:931–939. 2005. View Article : Google Scholar : PubMed/NCBI | |
Taheri F, Ochoa JB, Faghiri Z, Culotta K, Park HJ, Lan MS, Zea AH and Ochoa AC: l-Arginine regulates the expression of the T-cell receptor ζ chain (CD3ζ) in Jurkat cells. Clin Cancer Res. 7:958–965. 2001. | |
Bernard AC, Mistry SK, Morris SM Jr, O'Brien WE, Tsuei BJ, Maley ME, Shirley LA, Kearney PA, Boulanger BR and Ochoa JB: Alterations in arginine metabolic enzymes in trauma. Shock. 15:215–219. 2001. View Article : Google Scholar : PubMed/NCBI | |
Ichihara F, Kono K, Sekikawa T and Matsumoto Y: Surgical stress induces decreased expression of signal-transducing ζ molecules in T cells. Eur Surg Res. 31:138–146. 1999. View Article : Google Scholar : PubMed/NCBI | |
Park KG, Heys SD, Blessing K, Kelly P, McNurlan MA, Eremin O and Garlick PJ: Stimulation of human breast cancers by dietary L-arginine. Clin Sci. 82:413–417. 1992. View Article : Google Scholar : PubMed/NCBI | |
Pan PY, Zang Y, Weber K, Meseck ML and Chen SH: OX40 ligation enhances primary and memory cytotoxic T lymphocyte responses in an immunotherapy for hepatic colon metastases. Mol Ther. 6:528–536. 2002. View Article : Google Scholar : PubMed/NCBI | |
Makarenkova VP, Bansal V, Matta BM, Perez LA and Ochoa JB: CD11b+/Gr-1+ myeloid suppressor cells cause T cell dysfunction after traumatic stress. J Immunol. 176:2085–2094. 2006. View Article : Google Scholar : PubMed/NCBI | |
Yang L, DeBusk LM, Fukuda K, Fingleton B, Green-Jarvis B, Shyr Y, Matrisian LM, Carbone DP and Lin PC: Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell. 6:409–421. 2004. View Article : Google Scholar : PubMed/NCBI | |
Allegra A, Alonci A, Penna G, Innao V, Gerace D, Rotondo F and Musolino C: The cancer stem cell hypothesis: a guide to potential molecular targets. Cancer Invest. 32:470–495. 2014. View Article : Google Scholar : PubMed/NCBI | |
Ye XZ, Yu SC and Bian XW: Contribution of myeloid-derived suppressor cells to tumor-induced immune suppression, angiogenesis, invasion and metastasis. J Genet Genomics. 37:423–430. 2010. View Article : Google Scholar : PubMed/NCBI | |
Mantovani G, Macciò A, Madeddu C, Mura L, Gramignano G, Lusso MR, Massa E, Mocci M and Serpe R: Antioxidant agents are effective in inducing lymphocyte progression through cell cycle in advanced cancer patients: assessment of the most important laboratory indexes of cachexia and oxidative stress. J Mol Med. 81:664–673. 2003. View Article : Google Scholar : PubMed/NCBI | |
Szuster-Ciesielska A, Hryciuk-Umer E, Stepulak A, Kupisz K and Kandefer-Szerszeń M: Reactive oxygen species production by blood neutrophils of patients with laryngeal carcinoma and antioxidative enzyme activity in their blood. Acta Oncol. 43:252–258. 2004. View Article : Google Scholar : PubMed/NCBI | |
Bronte V, Kasic T, Gri G, Gallana K, Borsellino G, Marigo I, Battistini L, Iafrate M, Prayer-Galetti T, Pagano F, et al: Boosting antitumor responses of T lymphocytes infiltrating human prostate cancers. J Exp Med. 201:1257–1268. 2005. View Article : Google Scholar : PubMed/NCBI | |
Nagaraj S, Gupta K, Pisarev V, Kinarsky L, Sherman S, Kang L, Herber DL, Schneck J and Gabrilovich DI: Altered recognition of antigen is a mechanism of CD8+ T cell tolerance in cancer. Nat Med. 13:828–835. 2007. View Article : Google Scholar : PubMed/NCBI | |
Nagaraj S, Schrum AG, Cho HI, Celis E and Gabrilovich DI: Mechanism of T cell tolerance induced by myeloid-derived suppressor cells. J Immunol. 184:3106–3116. 2010. View Article : Google Scholar : PubMed/NCBI | |
Yan Z, Garg SK and Banerjee R: Regulatory T cells interfere with glutathione metabolism in dendritic cells and T cells. J Biol Chem. 285:41525–41532. 2010. View Article : Google Scholar : PubMed/NCBI | |
Yan Z, Garg SK, Kipnis J and Banerjee R: Extracellular redox modulation by regulatory T cells. Nat Chem Biol. 5:721–723. 2009. View Article : Google Scholar : PubMed/NCBI | |
Bronte V, Serafini P, Apolloni E and Zanovello P: Tumor-induced immune dysfunctions caused by myeloid suppressor cells. J Immunother. 24:431–446. 2001. View Article : Google Scholar : PubMed/NCBI | |
Salvadori S, Martinelli G and Zier K: Resection of solid tumors reverses T cell defects and restores protective immunity. J Immunol. 164:2214–2220. 2000. View Article : Google Scholar : PubMed/NCBI | |
Seung LP, Rowley DA, Dubey P and Schreiber H: Synergy between T-cell immunity and inhibition of paracrine stimulation causes tumor rejection. Proc Natl Acad Sci USA. 92:6254–6258. 1995. View Article : Google Scholar : PubMed/NCBI | |
Terabe M, Matsui S, Park JM, Mamura M, Noben-Trauth N, Donaldson DD, Chen W, Wahl SM, Ledbetter S, Pratt B, et al: Transforming growth factor-β production and myeloid cells are an effector mechanism through which CD1d-restricted T cells block cytotoxic T lymphocyte-mediated tumor immunosurveillance: abrogation prevents tumor recurrence. J Exp Med. 198:1741–1752. 2003. View Article : Google Scholar : PubMed/NCBI | |
Ugel S, Delpozzo F, Desantis G, Papalini F, Simonato F, Sonda N, Zilio S and Bronte V: Therapeutic targeting of myeloid-derived suppressor cells. Curr Opin Pharmacol. 9:470–481. 2009. View Article : Google Scholar : PubMed/NCBI | |
Nefedova Y, Fishman M, Sherman S, Wang X, Beg AA and Gabrilovich DI: Mechanism of all-trans retinoic acid effect on tumor-associated myeloid-derived suppressor cells. Cancer Res. 7:11021–11028. 2007. View Article : Google Scholar | |
Mirza N, Fishman M, Fricke I, Dunn M, Neuger AM, Frost TJ, Lush RM, Antonia S and Gabrilovich DI: All-trans-retinoic acid improves differentiation of myeloid cells and immune response in cancer patients. Cancer Res. 66:9299–9307. 2006. View Article : Google Scholar : PubMed/NCBI | |
Talmadge JE, Hood KC, Zobel LC, Shafer LR, Coles M and Toth B: Chemoprevention by cyclooxygenase-2 inhibition reduces immature myeloid suppressor cell expansion. Int Immunopharmacol. 7:140–151. 2007. View Article : Google Scholar : PubMed/NCBI | |
Suzuki E, Kapoor V, Jassar AS, Kaiser LR and Albelda SM: Gemcitabine selectively eliminates splenic Gr-1+/CD11b+ myeloid suppressor cells in tumor-bearing animals and enhances antitumor immune activity. Clin Cancer Res. 11:6713–6721. 2005. View Article : Google Scholar : PubMed/NCBI | |
Hotchkiss RS, Tinsley KW, Hui JJ, Chang KC, Swanson PE, Drewry AM, Buchman TG and Karl IE: p53-dependent and -independent pathways of apoptotic cell death in sepsis. J Immunol. 164:3675–3680. 2000. View Article : Google Scholar : PubMed/NCBI | |
Ding ZC, Lu X, Yu M, Lemos H, Huang L, Chandler P, Liu K, Walters M, Krasinski A, Mack M, et al: Immunosuppressive myeloid cells induced by chemotherapy attenuate antitumor CD4+ T-cell responses through the PD-1-PD-L1 axis. Cancer Res. 74:3441–3453. 2014. View Article : Google Scholar : PubMed/NCBI | |
Triozzi PL, Aldrich W and Singh A: Effects of interleukin-1 receptor antagonist on tumor stroma in experimental uveal melanoma. Invest Ophthalmol Vis Sci. 52:5529–5535. 2011. View Article : Google Scholar : PubMed/NCBI | |
Jiang J, Wang Z, Li Z, Zhang J, Wang C, Xu X and Qin Z: Early exposure of high-dose interleukin-4 to tumor stroma reverses myeloid cell-mediated T-cell suppression. Gene Ther. 17:991–999. 2010. View Article : Google Scholar : PubMed/NCBI | |
Ko JS, Zea AH, Rini BI, Ireland JL, Elson P, Cohen P, Golshayan A, Rayman PA, Wood L, Garcia J, et al: Sunitinib mediates reversal of myeloid-derived suppressor cell accumulation in renal cell carcinoma patients. Clin Cancer Res. 15:2148–2157. 2009. View Article : Google Scholar : PubMed/NCBI | |
Ko JS, Rayman P, Ireland J, Swaidani S, Li G, Bunting KD, Rini B, Finke JH and Cohen PA: Direct and differential suppression of myeloid-derived suppressor cell subsets by sunitinib is compartmentally constrained. Cancer Res. 70:3526–3536. 2010. View Article : Google Scholar : PubMed/NCBI | |
Pan PY, Wang GX, Yin B, Ozao J, Ku T, Divino CM and Chen SH: Reversion of immune tolerance in advanced malignancy: modulation of myeloid-derived suppressor cell development by blockade of stem-cell factor function. Blood. 111:219–228. 2008. View Article : Google Scholar : PubMed/NCBI | |
Gao P, Zhang H, Dinavahi R, Li F, Xiang Y, Raman V, Bhujwalla ZM, Felsher DW, Cheng L, Pevsner J, et al: HIF-dependent antitumorigenic effect of antioxidants in vivo. Cancer Cell. 12:230–238. 2007. View Article : Google Scholar : PubMed/NCBI | |
Hayes CS, Shicora AC, Keough MP, Snook AE, Burns MR and Gilmour SK: Polyamine-blocking therapy reverses immunosuppression in the tumor microenvironment. Cancer Immunol Res. 2:274–285. 2014. View Article : Google Scholar : PubMed/NCBI | |
Santilli G, Piotrowska I, Cantilena S, Chayka O, D'Alicarnasso M, Morgenstern DA, Himoudi N, Pearson K, Anderson J, Thrasher AJ, et al: Polyphenon [corrected] E enhances the antitumor immune response in neuroblastoma by inactivating myeloid suppressor cells. Clin Cancer Res. 19:1116–1125. 2013. View Article : Google Scholar : PubMed/NCBI | |
Serafini P, Meckel K, Kelso M, Noonan K, Califano J, Koch W, Dolcetti L, Bronte V and Borrello I: Phosphodiesterase-5 inhibition augments endogenous antitumor immunity by reducing myeloid-derived suppressor cell function. J Exp Med. 203:2691–2702. 2006. View Article : Google Scholar : PubMed/NCBI | |
Melani C, Sangaletti S, Barazzetta FM, Werb Z and Colombo MP: Amino-biphosphonate-mediated MMP-9 inhibition breaks the tumor-bone marrow axis responsible for myeloid-derived suppressor cell expansion and macrophage infiltration in tumor stroma. Cancer Res. 67:11438–11446. 2007. View Article : Google Scholar : PubMed/NCBI | |
Valenti R, Huber V, Filipazzi P, Pilla L, Sovena G, Villa A, Corbelli A, Fais S, Parmiani G and Rivoltini L: Human tumor-released microvesicles promote the differentiation of myeloid cells with transforming growth factor-β-mediated suppressive activity on T lymphocytes. Cancer Res. 66:9290–9298. 2006. View Article : Google Scholar : PubMed/NCBI | |
Ghoreschi K, Laurence A and O'Shea JJ: Selectivity and therapeutic inhibition of kinases: to be or not to be? Nat Immunol. 10:356–360. 2009. View Article : Google Scholar : PubMed/NCBI | |
Egberts F, Kahler KC, Livingstone E and Hauschild A: Metastatic melanoma: scientific rationale for sorafenib treatment and clinical results. Onkologie. 31:398–403. 2008. View Article : Google Scholar : PubMed/NCBI | |
Motzer RJ, Michaelson MD, Redman BG, Hudes GR, Wilding G, Figlin RA, Ginsberg MS, Kim ST, Baum CM, DePrimo SE, et al: Activity of SU11248, a multitargeted inhibitor of vascular endothelial growth factor receptor and platelet-derived growth factor receptor, in patients with metastatic renal cell carcinoma. J Clin Oncol. 24:16–24. 2006. View Article : Google Scholar : PubMed/NCBI | |
Motzer RJ, Rini BI, Bukowski RM, Curti BD, George DJ, Hudes GR, Redman BG, Margolin KA, Merchan JR, Wilding G, et al: Sunitinib in patients with metastatic renal cell carcinoma. JAMA. 295:2516–2524. 2006. View Article : Google Scholar : PubMed/NCBI | |
Motzer RJ and Bukowski RM: Targeted therapy for metastatic renal cell carcinoma. J Clin Oncol. 24:5601–5608. 2006. View Article : Google Scholar : PubMed/NCBI | |
Ozao-Choy J, Ma G, Kao J, Wang GX, Meseck M, Sung M, Schwartz M, Divino CM, Pan PY and Chen SH: The novel role of tyrosine kinase inhibitor in the reversal of immune suppression and modulation of tumor microenvironment for immune-based cancer therapies. Cancer Res. 69:2514–2522. 2009. View Article : Google Scholar : PubMed/NCBI | |
van Cruijsen H, Hoekman K, Stam AG, van den Eertwegh AJ, Kuenen BC, Scheper RJ, Giaccone G and de Gruijl TD: Defective differentiation of myeloid and plasmacytoid dendritic cells in advanced cancer patients is not normalized by tyrosine kinase inhibition of the vascular endothelial growth factor receptor. Clin Dev Immunol. 2007:173152007. View Article : Google Scholar : PubMed/NCBI | |
Xin H, Zhang C, Herrmann A, Du Y, Figlin R and Yu H: Sunitinib inhibition of Stat3 induces renal cell carcinoma tumor cell apoptosis and reduces immunosuppressive cells. Cancer Res. 69:2506–2513. 2009. View Article : Google Scholar : PubMed/NCBI | |
Bose A, Taylor JL, Alber S, Watkins SC, Garcia JA, Rini BI, Ko JS, Cohen PA, Finke JH and Storkus WJ: Sunitinib facilitates the activation and recruitment of therapeutic anti-tumor immunity in concert with specific vaccination. Int J Cancer. 129:2158–2170. 2011. View Article : Google Scholar : PubMed/NCBI | |
North RJ: Down-regulation of the antitumor immune response. Adv Cancer Res. 45:1–43. 1985. View Article : Google Scholar : PubMed/NCBI | |
Hart KM, Usherwood EJ and Berwin BL: CX3CR1 delineates temporally and functionally distinct subsets of myeloid-derived suppressor cells in a mouse model of ovarian cancer. Immunol Cell Biol. 92:499–508. 2014. View Article : Google Scholar : PubMed/NCBI | |
Huang B, Pan PY, Li Q, Sato AI, Levy DE, Bromberg J, Divino CM and Chen SH: Gr-1+CD115+ immature myeloid suppressor cells mediate the development of tumor-induced T regulatory cells and T-cell anergy in tumor-bearing host. Cancer Res. 66:1123–1131. 2006. View Article : Google Scholar : PubMed/NCBI | |
Tomihara K, Guo M and Shin T, Sun X, Ludwig SM, Brumlik MJ, Zhang B, Curiel TJ and Shin T: Antigen-specific immunity and cross-priming by epithelial ovarian carcinoma-induced CD11b(+)Gr-1(+) cells. J Immunol. 184:6151–6160. 2010. View Article : Google Scholar : PubMed/NCBI | |
Ko HJ, Lee JM, Kim YJ, Kim YS, Lee KA and Kang CY: Immunosuppressive myeloid-derived suppressor cells can be converted into immunogenic APCs with the help of activated NKT cells: an alternative cell-based antitumor vaccine. J Immunol. 182:1818–1828. 2009. View Article : Google Scholar : PubMed/NCBI | |
Nausch N, Galani IE, Schlecker E and Cerwenka A: Mononuclear myeloid-derived ‘suppressor’ cells express RAE-1 and activate natural killer cells. Blood. 112:4080–4089. 2008. View Article : Google Scholar : PubMed/NCBI | |
Greifenberg V, Ribechini E, Rössner S and Lutz MB: Myeloid-derived suppressor cell activation by combined LPS and IFN-γ treatment impairs DC development. Eur J Immunol. 39:2865–2876. 2009. View Article : Google Scholar : PubMed/NCBI | |
Dolcetti L, Peranzoni E, Ugel S, Marigo I, Gomez A Fernandez, Mesa C, Geilich M, Winkels G, Traggiai E, Casati A, et al: Hierarchy of immunosuppressive strength among myeloid-derived suppressor cell subsets is determined by GM-CSF. Eur J Immunol. 40:22–35. 2010. View Article : Google Scholar : PubMed/NCBI | |
Bronte V: Myeloid-derived suppressor cells in inflammation: uncovering cell subsets with enhanced immunosuppressive functions. Eur J Immunol. 39:2670–2672. 2009. View Article : Google Scholar : PubMed/NCBI | |
Lioubin MN, Algate PA, Tsai S, Carlberg K, Aebersold A and Rohrschneider LR: p150Ship, a signal transduction molecule with inositol polyphosphate-5-phosphatase activity. Genes Dev. 10:1084–1095. 1996. View Article : Google Scholar : PubMed/NCBI | |
Helgason CD, Damen JE, Rosten P, Grewal R, Sorensen P, Chappel SM, Borowski A, Jirik F, Krystal G and Humphries RK: Targeted disruption of SHIP leads to hemopoietic perturbations, lung pathology, and a shortened life span. Genes Dev. 12:1610–1620. 1998. View Article : Google Scholar : PubMed/NCBI | |
Rauh MJ, Ho V, Pereira C, Sham A, Sly LM, Lam V, Huxham L, Minchinton AI, Mui A and Krystal G: SHIP represses the generation of alternatively activated macrophages. Immunity. 23:361–374. 2005. View Article : Google Scholar : PubMed/NCBI | |
Paraiso KHT, Ghansah T, Costello A, Engelman RW and Kerr WG: Induced SHIP deficiency expands myeloid regulatory cells and abrogates graft-versus-host disease. J Immunol. 178:2893–2900. 2007. View Article : Google Scholar : PubMed/NCBI | |
Guedez L, Jensen-Taubman S, Bourboulia D, Kwityn CJ, Wei B, Caterina J and Stetler-Stevenson WG: TIMP-2 targets tumor-associated myeloid suppressor cells with effects in cancer immune dysfunction and angiogenesis. J Immunother. 35:502–512. 2012. View Article : Google Scholar : PubMed/NCBI | |
Kaimala S, Mohamed YA, Nader N, Issac J, Elkord E, Chouaib S, Fernandez-Cabezudo MJ and Al-Ramadi BK: Salmonella-mediated tumor regression involves targeting of tumor myeloid suppressor cells causing a shift to M1-like phenotype and reduction in suppressive capacity. Cancer Immunol Immunother. 63:587–599. 2014. View Article : Google Scholar : PubMed/NCBI |