Myeloid suppressor cells in cancer and autoimmunity

Journal of Autoimmunity

Volumn 85, Issue , 2017, Pages 117-125

  Sica, Antonio ^a,b   Massarotti, Marco ^b,c  

^a UNIVERSITY OF EASTERN PIEDMONT   (Italy)

^b HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^c ROYAL LANCASTER INFIRMARY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE;

ANGIOGENESIS; ANTIINFLAMMATORY ACTIVITY; AUTOIMMUNE DISEASE; AUTOIMMUNITY; BENIGN NEOPLASM; BONE MARROW CELL; CANCER IMMUNOTHERAPY; CELL DIFFERENTIATION; CELL PLASTICITY; CYTOTOXICITY; HUMAN; IMMUNOSUPPRESSIVE TREATMENT; INFLAMMATION; LYMPHANGIOGENESIS; MACROPHAGE ACTIVATION; MALIGNANT NEOPLASM; MICROFLORA; MYELOID-DERIVED SUPPRESSOR CELL; NONHUMAN; PHYSIOLOGICAL PROCESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; SIGNAL TRANSDUCTION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR GROWTH; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; ANIMAL; CELL PROLIFERATION; IMMUNOLOGY; IMMUNOTHERAPY; NEOPLASM; PHYSIOLOGY; PROCEDURES;

ANIMALS; AUTOIMMUNITY; CELL PROLIFERATION; HUMANS; IMMUNOSUPPRESSION; IMMUNOTHERAPY; MYELOID CELLS; MYELOID-DERIVED SUPPRESSOR CELLS; NEOPLASMS;

EID: 85024402294     PISSN: 08968411     EISSN: 10959157     Source Type: Journal    
DOI: 10.1016/j.jaut.2017.07.010     Document Type: Review

References (107)

1. Shalapour, S., Karin, M., Immunity, inflammation, and cancer: an eternal fight between good and evil. J. Clin. Investig. 125:9 (2015), 3347–3355.
2. Ugel, S., De Sanctis, F., Mandruzzato, S., Bronte, V., Tumor-induced myeloid deviation: when myeloid-derived suppressor cells meet tumor-associated macrophages. J. Clin. Investig. 125:9 (2015), 3365–3376.
3. Mantovani, A., Sica, A., Macrophages, innate immunity and cancer: balance, tolerance, and diversity. Curr. Opin. Immunol. 22:2 (2010), 231–237.
4. Sica, A., Mantovani, A., Macrophage plasticity and polarization: in vivo veritas. J. Clin. Investig. 122:3 (2012), 787–795.
5. Sica, A., Erreni, M., Allavena, P., Porta, C., Macrophage polarization in pathology. Cell Mol. Life Sci. 72:21 (2015), 4111–4126.
6. Bjorkgren, I., Gylling, H., Turunen, H., Huhtaniemi, I., Strauss, L., Poutanen, M., Sipila, P., Imbalanced lipid homeostasis in the conditional Dicer1 knockout mouse epididymis causes instability of the sperm membrane. FASEB J. 29:2 (2015), 433–442.
7. Mantovani, A., Allavena, P., Sica, A., Balkwill, F., Cancer-related inflammation. Nature 454:7203 (2008), 436–444.
8. Rojas, A., Jiang, J., Ganesh, T., Yang, M.S., Lelutiu, N., Gueorguieva, P., Dingledine, R., Cyclooxygenase-2 in epilepsy. Epilepsia 55:1 (2014), 17–25.
9. Bronte, V., Brandau, S., Chen, S.H., Colombo, M.P., Frey, A.B., Greten, T.F., Mandruzzato, S., Murray, P.J., Ochoa, A., Ostrand-Rosenberg, S., Rodriguez, P.C., Sica, A., Umansky, V., Vonderheide, R.H., Gabrilovich, D.I., Recommendations for myeloid-derived suppressor cell nomenclature and characterization standards. Nat. Commun., 7, 2016, 12150.
10. Sica, A., Strauss, L., Energy metabolism drives myeloid-derived suppressor cell differentiation and functions in pathology. J. Leukoc. Biol. 35 (2017 Jun), 27–35.
11. Conde, P., Rodriguez, M., van der Touw, W., Jimenez, A., Burns, M., Miller, J., Brahmachary, M., Chen, H.M., Boros, P., Rausell-Palamos, F., Yun, T.J., Riquelme, P., Rastrojo, A., Aguado, B., Stein-Streilein, J., Tanaka, M., Zhou, L., Zhang, J., Lowary, T.L., Ginhoux, F., Park, C.G., Cheong, C., Brody, J., Turley, S.J., Lira, S.A., Bronte, V., Gordon, S., Heeger, P.S., Merad, M., Hutchinson, J., Chen, S.H., Ochando, J., DC-SIGN(+) macrophages control the induction of transplantation tolerance. Immunity 42:6 (2015), 1143–1158.
12. Zoso, A., Mazza, E.M., Bicciato, S., Mandruzzato, S., Bronte, V., Serafini, P., Inverardi, L., Human fibrocytic myeloid-derived suppressor cells express IDO and promote tolerance via Treg-cell expansion. Eur. J. Immunol. 44:11 (2014), 3307–3319.
13. Gabrilovich, D.I., Ostrand-Rosenberg, S., Bronte, V., Coordinated regulation of myeloid cells by tumours. Nat. Rev. Immunol. 12:4 (2012), 253–268.
14. Hanahan, D., Weinberg, R.A., Hallmarks of cancer: the next generation. Cell 144:5 (2011), 646–674.
15. Allen, E., Walters, I.B., Hanahan, D., Brivanib, a dual FGF/VEGF inhibitor, is active both first and second line against mouse pancreatic neuroendocrine tumors developing adaptive/evasive resistance to VEGF inhibition. Clin. Cancer Res. 17:16 (2011), 5299–5310.
16. Kalisperati, P., Spanou, E., Pateras, I.S., Korkolopoulou, P., Varvarigou, A., Karavokyros, I., Gorgoulis, V.G., Vlachoyiannopoulos, P.G., Sougioultzis, S., Inflammation, DNA damage, Helicobacter pylori and gastric tumorigenesis. Front. Genet., 8, 2017, 20.
17. Tudek, B., Zdzalik-Bielecka, D., Tudek, A., Kosicki, K., Fabisiewicz, A., Speina, E., Lipid peroxidation in face of DNA damage, DNA repair and other cellular processes. Free Radic. Biol. Med. 107 (2017), 77–89.
18. Ueha, S., Shand, F.H., Matsushima, K., Myeloid cell population dynamics in healthy and tumor-bearing mice. Int. Immunopharmacol. 11:7 (2011), 783–788.
19. Strauss, L., Sangaletti, S., Consonni, F.M., Szebeni, G., Morlacchi, S., Totaro, M.G., Porta, C., Anselmo, A., Tartari, S., Doni, A., Zitelli, F., Tripodo, C., Colombo, M.P., Sica, A., RORC1 regulates tumor-promoting “emergency” granulo-monocytopoiesis. Cancer Cell 28:2 (2015), 253–269.
20. Metcalf, D., Hematopoietic cytokines. Blood 111:2 (2008), 485–491.
21. Carmichael, C.L., Majewski, I.J., Alexander, W.S., Metcalf, D., Hilton, D.J., Hewitt, C.A., Scott, H.S., Hematopoietic defects in the Ts1Cje mouse model of Down syndrome. Blood 113:9 (2009), 1929–1937.
22. Hume, D.A., MacDonald, K.P., Therapeutic applications of macrophage colony-stimulating factor-1 (CSF-1) and antagonists of CSF-1 receptor (CSF-1R) signaling. Blood 119:8 (2012), 1810–1820.
23. Endale Ahanda, M.L., Fritz, E.R., Estelle, J., Hu, Z.L., Madsen, O., Groenen, M.A., Beraldi, D., Kapetanovic, R., Hume, D.A., Rowland, R.R., Lunney, J.K., Rogel-Gaillard, C., Reecy, J.M., Giuffra, E., Prediction of altered 3′- UTR miRNA-binding sites from RNA-Seq data: the swine leukocyte antigen complex (SLA) as a model region. PLoS One, 7(11), 2012, e48607.
24. Akagi, T., Saitoh, T., O'Kelly, J., Akira, S., Gombart, A.F., Koeffler, H.P., Impaired response to GM-CSF and G-CSF, and enhanced apoptosis in C/EBPbeta-deficient hematopoietic cells. Blood 111:6 (2008), 2999–3004.
25. Akagi, T., Luong, Q.T., Gui, D., Said, J., Selektar, J., Yung, A., Bunce, C.M., Braunstein, G.D., Koeffler, H.P., Induction of sodium iodide symporter gene and molecular characterisation of HNF3 beta/FoxA2, TTF-1 and C/EBP beta in thyroid carcinoma cells. Br. J. Cancer 99:5 (2008), 781–788.
26. Zhang, R., Ito, S., Nishio, N., Cheng, Z., Suzuki, H., Isobe, K., Up-regulation of Gr1+CD11b+ population in spleen of dextran sulfate sodium administered mice works to repair colitis. Inflamm. Allergy Drug Targets 10:1 (2011), 39–46.
27. Friedman, A.D., Transcriptional control of granulocyte and monocyte development. Oncogene 26:47 (2007), 6816–6828.
28. Cai, D.H., Wang, D., Keefer, J., Yeamans, C., Hensley, K., Friedman, A.D., C/EBP alpha:AP-1 leucine zipper heterodimers bind novel DNA elements, activate the PU.1 promoter and direct monocyte lineage commitment more potently than C/EBP alpha homodimers or AP-1. Oncogene 27:19 (2008), 2772–2779.
29. Allavena, P., Mantovani, A., Immunology in the clinic review series; focus on cancer: tumour-associated macrophages: undisputed stars of the inflammatory tumour microenvironment. Clin. Exp. Immunol. 167:2 (2012), 195–205.
30. Mantovani, A., Biswas, S.K., Galdiero, M.R., Sica, A., Locati, M., Macrophage plasticity and polarization in tissue repair and remodelling. J. Pathol. 229:2 (2013), 176–185.
31. Tolentino, Y.F., Elia, P.P., Fogaca, H.S., Carneiro, A.J., Zaltman, C., Moura-Neto, R., Luiz, R.R., Carvalho Mda, G., de Souza, H.S., Common NOD2/CARD15 and TLR4 polymorphisms are associated with Crohn's disease phenotypes in southeastern Brazilians. Dig. Dis. Sci. 61:9 (2016), 2636–2647.
32. Biswas, S.K., Mantovani, A., Orchestration of metabolism by macrophages. Cell Metab. 15:4 (2012), 432–437.
33. Swirski, F.K., Nahrendorf, M., Etzrodt, M., Wildgruber, M., Cortez-Retamozo, V., Panizzi, P., Figueiredo, J.L., Kohler, R.H., Chudnovskiy, A., Waterman, P., Aikawa, E., Mempel, T.R., Libby, P., Weissleder, R., Pittet, M.J., Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science 325:5940 (2009), 612–616.
34. Christen, T., Nahrendorf, M., Wildgruber, M., Swirski, F.K., Aikawa, E., Waterman, P., Shimizu, K., Weissleder, R., Libby, P., Molecular imaging of innate immune cell function in transplant rejection. Circulation 119:14 (2009), 1925–1932.
35. Sindrilaru, A., Peters, T., Wieschalka, S., Baican, C., Baican, A., Peter, H., Hainzl, A., Schatz, S., Qi, Y., Schlecht, A., Weiss, J.M., Wlaschek, M., Sunderkotter, C., Scharffetter-Kochanek, K., An unrestrained proinflammatory M1 macrophage population induced by iron impairs wound healing in humans and mice. J. Clin. Investig. 121:3 (2011), 985–997.
36. Boyle, K.B., Gyori, D., Sindrilaru, A., Scharffetter-Kochanek, K., Taylor, P.R., Mocsai, A., Stephens, L.R., Hawkins, P.T., Class IA phosphoinositide 3-kinase beta and delta regulate neutrophil oxidase activation in response to Aspergillus fumigatus hyphae. J. Immunol. 186:5 (2011), 2978–2989.
37. Jemaa, M., Galluzzi, L., Kepp, O., Boileve, A., Lissa, D., Senovilla, L., Harper, F., Pierron, G., Berardinelli, F., Antoccia, A., Castedo, M., Vitale, I., Kroemer, G., Preferential killing of p53-deficient cancer cells by reversine. Cell Cycle 11:11 (2012), 2149–2158.
38. Mantovani, A., Marchesi, F., Malesci, A., Laghi, L., Allavena, P., Tumour-associated macrophages as treatment targets in oncology. Nat. Rev. Clin. Oncol. 14:7 (2017), 399–416.
39. Perl, A., Activation of mTOR (mechanistic target of rapamycin) in rheumatic diseases. Nat. Rev. Rheumatol. 12:3 (2016), 169–182.
40. Cuda, C.M., Pope, R.M., Perlman, H., The inflammatory role of phagocyte apoptotic pathways in rheumatic diseases. Nat. Rev. Rheumatol. 12:9 (2016), 543–558.
41. Heo, J.S., Park, J.S., Lee, E.J., Kim, T.H., Jang, A.S., Park, S.W., Kim, J.N., Kim, Y.G., Uh, S.T., Choi, J.S., Na, J.O., Kim, Y.H., Jeong, S.H., Kim, Y.B., Kim, S.R., Park, C.S., Retinoic acid receptor alpha: one of plasma biomarkers associated with exacerbation of chronic obstructive pulmonary disease. COPD 11:2 (2014), 152–162.
42. Hammami, I., Chen, J., Murschel, F., Bronte, V., De Crescenzo, G., Jolicoeur, M., Immunosuppressive activity enhances central carbon metabolism and bioenergetics in myeloid-derived suppressor cells in vitro models. BMC Cell Biol., 13, 2012, 18.
43. Nefedova, Y., Huang, M., Kusmartsev, S., Bhattacharya, R., Cheng, P., Salup, R., Jove, R., Gabrilovich, D., Hyperactivation of STAT3 is involved in abnormal differentiation of dendritic cells in cancer. J. Immunol. 172:1 (2004), 464–474.
44. Trikha, P., Carson, W.E. 3rd, Signaling pathways involved in MDSC regulation. Biochim. Biophys. Acta 1846:1 (2014), 55–65.
45. Kumar, V., Cheng, P., Condamine, T., Mony, S., Languino, L.R., McCaffrey, J.C., Hockstein, N., Guarino, M., Masters, G., Penman, E., Denstman, F., Xu, X., Altieri, D.C., Du, H., Yan, C., Gabrilovich, D.I., CD45 phosphatase inhibits STAT3 transcription factor activity in myeloid cells and promotes tumor-associated macrophage differentiation. Immunity 44:2 (2016), 303–315.
46. Stromnes, I.M., Schmitt, T.M., Chapuis, A.G., Hingorani, S.R., Greenberg, P.D., Re-adapting T cells for cancer therapy: from mouse models to clinical trials. Immunol. Rev. 257:1 (2014), 145–164.
47. Diaz-Montero, C.M., Salem, M.L., Nishimura, M.I., Garrett-Mayer, E., Cole, D.J., Montero, A.J., Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin-cyclophosphamide chemotherapy. Cancer Immunol. Immunother. 58:1 (2009), 49–59.
48. Lahmar, Q., Keirsse, J., Laoui, D., Movahedi, K., Van Overmeire, E., Van Ginderachter, J.A., Tissue-resident versus monocyte-derived macrophages in the tumor microenvironment. Biochim. Biophys. Acta 1865:1 (2016), 23–34.
49. Qian, B.Z., Li, J., Zhang, H., Kitamura, T., Zhang, J., Campion, L.R., Kaiser, E.A., Snyder, L.A., Pollard, J.W., CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature 475:7355 (2011), 222–225.
50. Wynn, T.A., Chawla, A., Pollard, J.W., Macrophage biology in development, homeostasis and disease. Nature 496:7446 (2013), 445–455.
51. Jenkins, S.J., Ruckerl, D., Cook, P.C., Jones, L.H., Finkelman, F.D., van Rooijen, N., MacDonald, A.S., Allen, J.E., Local macrophage proliferation, rather than recruitment from the blood, is a signature of TH2 inflammation. Science 332:6035 (2011), 1284–1288.
52. Sica, A., Bronte, V., Altered macrophage differentiation and immune dysfunction in tumor development. J. Clin. Investig. 117:5 (2007), 1155–1166.
53. Cui, T.X., Kryczek, I., Zhao, L., Zhao, E., Kuick, R., Roh, M.H., Vatan, L., Szeliga, W., Mao, Y., Thomas, D.G., Kotarski, J., Tarkowski, R., Wicha, M., Cho, K., Giordano, T., Liu, R., Zou, W., Myeloid-derived suppressor cells enhance stemness of cancer cells by inducing microRNA101 and suppressing the corepressor CtBP2. Immunity 39:3 (2013), 611–621.
54. Balmer, M.L., Schurch, C.M., Saito, Y., Geuking, M.B., Li, H., Cuenca, M., Kovtonyuk, L.V., McCoy, K.D., Hapfelmeier, S., Ochsenbein, A.F., Manz, M.G., Slack, E., Macpherson, A.J., Microbiota-derived compounds drive steady-state granulopoiesis via MyD88/TICAM signaling. J. Immunol. 193:10 (2014), 5273–5283.
55. Deshmukh, H.S., Liu, Y., Menkiti, O.R., Mei, J., Dai, N., O'Leary, C.E., Oliver, P.M., Kolls, J.K., Weiser, J.N., Worthen, G.S., The microbiota regulates neutrophil homeostasis and host resistance to Escherichia coli K1 sepsis in neonatal mice. Nat. Med. 20:5 (2014), 524–530.
56. Hill, D.A., Siracusa, M.C., Abt, M.C., Kim, B.S., Kobuley, D., Kubo, M., Kambayashi, T., Larosa, D.F., Renner, E.D., Orange, J.S., Bushman, F.D., Artis, D., Commensal bacteria-derived signals regulate basophil hematopoiesis and allergic inflammation. Nat. Med. 18:4 (2012), 538–546.
57. Khosravi, A., Yanez, A., Price, J.G., Chow, A., Merad, M., Goodridge, H.S., Mazmanian, S.K., Gut microbiota promote hematopoiesis to control bacterial infection. Cell Host Microbe 15:3 (2014), 374–381.
58. Trompette, A., Gollwitzer, E.S., Yadava, K., Sichelstiel, A.K., Sprenger, N., Ngom-Bru, C., Blanchard, C., Junt, T., Nicod, L.P., Harris, N.L., Marsland, B.J., Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat. Med. 20:2 (2014), 159–166.
59. Zhang, D., Chen, G., Manwani, D., Mortha, A., Xu, C., Faith, J.J., Burk, R.D., Kunisaki, Y., Jang, J.E., Scheiermann, C., Merad, M., Frenette, P.S., Neutrophil ageing is regulated by the microbiome. Nature 525:7570 (2015), 528–532.
60. Erny, D., Hrabe de Angelis, A.L., Jaitin, D., Wieghofer, P., Staszewski, O., David, E., Keren-Shaul, H., Mahlakoiv, T., Jakobshagen, K., Buch, T., Schwierzeck, V., Utermohlen, O., Chun, E., Garrett, W.S., McCoy, K.D., Diefenbach, A., Staeheli, P., Stecher, B., Amit, I., Prinz, M., Host microbiota constantly control maturation and function of microglia in the CNS. Nat. Neurosci. 18:7 (2015), 965–977.
61. Tamoutounour, S., Guilliams, M., Montanana Sanchis, F., Liu, H., Terhorst, D., Malosse, C., Pollet, E., Ardouin, L., Luche, H., Sanchez, C., Dalod, M., Malissen, B., Henri, S., Origins and functional specialization of macrophages and of conventional and monocyte-derived dendritic cells in mouse skin. Immunity 39:5 (2013), 925–938.
62. Kim, Y.G., Udayanga, K.G., Totsuka, N., Weinberg, J.B., Nunez, G., Shibuya, A., Gut dysbiosis promotes M2 macrophage polarization and allergic airway inflammation via fungi-induced PGE(2). Cell Host Microbe 15:1 (2014), 95–102.
63. Bain, C.C., Bravo-Blas, A., Scott, C.L., Gomez Perdiguero, E., Geissmann, F., Henri, S., Malissen, B., Osborne, L.C., Artis, D., Mowat, A.M., Constant replenishment from circulating monocytes maintains the macrophage pool in the intestine of adult mice. Nat. Immunol. 15:10 (2014), 929–937.
64. Singh, N., Gurav, A., Sivaprakasam, S., Brady, E., Padia, R., Shi, H., Thangaraju, M., Prasad, P.D., Manicassamy, S., Munn, D.H., Lee, J.R., Offermanns, S., Ganapathy, V., Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis. Immunity 40:1 (2014), 128–139.
65. Chang, P.V., Hao, L., Offermanns, S., Medzhitov, R., The microbial metabolite butyrate regulates intestinal macrophage function via histone deacetylase inhibition. Proc. Natl. Acad. Sci. U. S. A. 111:6 (2014), 2247–2252.
66. Muller, P.A., Koscso, B., Rajani, G.M., Stevanovic, K., Berres, M.L., Hashimoto, D., Mortha, A., Leboeuf, M., Li, X.M., Mucida, D., Stanley, E.R., Dahan, S., Margolis, K.G., Gershon, M.D., Merad, M., Bogunovic, M., Crosstalk between muscularis macrophages and enteric neurons regulates gastrointestinal motility. Cell 158:2 (2014), 300–313.
67. Fonseca, D.M., Hand, T.W., Han, S.J., Gerner, M.Y., Glatman Zaretsky, A., Byrd, A.L., Harrison, O.J., Ortiz, A.M., Quinones, M., Trinchieri, G., Brenchley, J.M., Brodsky, I.E., Germain, R.N., Randolph, G.J., Belkaid, Y., Microbiota-dependent sequelae of acute infection compromise tissue-specific immunity. Cell 163:2 (2015), 354–366.
68. Schwab, L., Goroncy, L., Palaniyandi, S., Gautam, S., Triantafyllopoulou, A., Mocsai, A., Reichardt, W., Karlsson, F.J., Radhakrishnan, S.V., Hanke, K., Schmitt-Graeff, A., Freudenberg, M., von Loewenich, F.D., Wolf, P., Leonhardt, F., Baxan, N., Pfeifer, D., Schmah, O., Schonle, A., Martin, S.F., Mertelsmann, R., Duyster, J., Finke, J., Prinz, M., Henneke, P., Hacker, H., Hildebrandt, G.C., Hacker, G., Zeiser, R., Neutrophil granulocytes recruited upon translocation of intestinal bacteria enhance graft-versus-host disease via tissue damage. Nat. Med. 20:6 (2014), 648–654.
69. Sawa, S., Cherrier, M., Lochner, M., Satoh-Takayama, N., Fehling, H.J., Langa, F., Di Santo, J.P., Eberl, G., Lineage relationship analysis of RORgammat+ innate lymphoid cells. Science 330:6004 (2010), 665–669.
70. Thaiss, C.A., Zmora, N., Levy, M., Elinav, E., The microbiome and innate immunity. Nature 535:7610 (2016), 65–74.
71. Rakoff-Nahoum, S., Paglino, J., Eslami-Varzaneh, F., Edberg, S., Medzhitov, R., Recognition of commensal microflora by toll-like receptors is required for intestinal homeostasis. Cell 118:2 (2004), 229–241.
72. Diard, M., Bakkeren, E., Cornuault, J.K., Moor, K., Hausmann, A., Sellin, M.E., Loverdo, C., Aertsen, A., Ackermann, M., De Paepe, M., Slack, E., Hardt, W.D., Inflammation boosts bacteriophage transfer between Salmonella spp. Science 355:6330 (2017), 1211–1215.
73. Gorjifard, S., Goldszmid, R.S., Microbiota-myeloid cell crosstalk beyond the gut. J. Leukoc. Biol. 100:5 (2016), 865–879.
74. Chirdo, F.G., Millington, O.R., Beacock-Sharp, H., Mowat, A.M., Immunomodulatory dendritic cells in intestinal lamina propria. Eur. J. Immunol. 35:6 (2005), 1831–1840.
75. Hart, A.L., Al-Hassi, H.O., Rigby, R.J., Bell, S.J., Emmanuel, A.V., Knight, S.C., Kamm, M.A., Stagg, A.J., Characteristics of intestinal dendritic cells in inflammatory bowel diseases. Gastroenterology 129:1 (2005), 50–65.
76. Hrncir, T., Stepankova, R., Kozakova, H., Hudcovic, T., Tlaskalova-Hogenova, H., Gut microbiota and lipopolysaccharide content of the diet influence development of regulatory T cells: studies in germ-free mice. BMC Immunol., 9, 2008, 65.
77. Wen, Z., Fiocchi, C., Inflammatory bowel disease: autoimmune or immune-mediated pathogenesis?. Clin. Dev. Immunol. 11:3–4 (2004), 195–204.
78. Ji, Y., Sun, S., Goodrich, J.K., Kim, H., Poole, A.C., Duhamel, G.E., Ley, R.E., Qi, L., Diet-induced alterations in gut microflora contribute to lethal pulmonary damage in TLR2/TLR4-deficient mice. Cell Rep. 8:1 (2014), 137–149.
79. Kostic, A.D., Gevers, D., Siljander, H., Vatanen, T., Hyotylainen, T., Hamalainen, A.M., Peet, A., Tillmann, V., Poho, P., Mattila, I., Lahdesmaki, H., Franzosa, E.A., Vaarala, O., de Goffau, M., Harmsen, H., Ilonen, J., Virtanen, S.M., Clish, C.B., Oresic, M., Huttenhower, C., Knip, M., Group, D.S., Xavier, R.J., The dynamics of the human infant gut microbiome in development and in progression toward type 1 diabetes. Cell Host Microbe 17:2 (2015), 260–273.
80. Scher, J.U., Abramson, S.B., The microbiome and rheumatoid arthritis. Nat. Rev. Rheumatol. 7:10 (2011), 569–578.
81. Scher, J.U., Ubeda, C., Artacho, A., Attur, M., Isaac, S., Reddy, S.M., Marmon, S., Neimann, A., Brusca, S., Patel, T., Manasson, J., Pamer, E.G., Littman, D.R., Abramson, S.B., Decreased bacterial diversity characterizes the altered gut microbiota in patients with psoriatic arthritis, resembling dysbiosis in inflammatory bowel disease. Arthritis Rheumatol. 67:1 (2015), 128–139.
82. Breban, M., Tap, J., Leboime, A., Said-Nahal, R., Langella, P., Chiocchia, G., Furet, J.P., Sokol, H., Faecal microbiota study reveals specific dysbiosis in spondyloarthritis. Ann. Rheum. Dis. 342:6161 (2013 Nov 22), 967–970.
83. Iida, N., Dzutsev, A., Stewart, C.A., Smith, L., Bouladoux, N., Weingarten, R.A., Molina, D.A., Salcedo, R., Back, T., Cramer, S., Dai, R.M., Kiu, H., Cardone, M., Naik, S., Patri, A.K., Wang, E., Marincola, F.M., Frank, K.M., Belkaid, Y., Trinchieri, G., Goldszmid, R.S., Commensal bacteria control cancer response to therapy by modulating the tumor microenvironment. Science 342:6161 (2013), 967–970.
84. Sivan, A., Corrales, L., Hubert, N., Williams, J.B., Aquino-Michaels, K., Earley, Z.M., Benyamin, F.W., Lei, Y.M., Jabri, B., Alegre, M.L., Chang, E.B., Gajewski, T.F., Commensal Bifidobacterium promotes antitumor immunity and facilitates anti-PD-L1 efficacy. Science 350:6264 (2015), 1084–1089.
85. Vetizou, M., Pitt, J.M., Daillere, R., Lepage, P., Waldschmitt, N., Flament, C., Rusakiewicz, S., Routy, B., Roberti, M.P., Duong, C.P., Poirier-Colame, V., Roux, A., Becharef, S., Formenti, S., Golden, E., Cording, S., Eberl, G., Schlitzer, A., Ginhoux, F., Mani, S., Yamazaki, T., Jacquelot, N., Enot, D.P., Berard, M., Nigou, J., Opolon, P., Eggermont, A., Woerther, P.L., Chachaty, E., Chaput, N., Robert, C., Mateus, C., Kroemer, G., Raoult, D., Boneca, I.G., Carbonnel, F., Chamaillard, M., Zitvogel, L., Anticancer immunotherapy by CTLA-4 blockade relies on the gut microbiota. Science 350:6264 (2015), 1079–1084.
86. Crook, K.R., Liu, P., Role of myeloid-derived suppressor cells in autoimmune disease. World J. Immunol. 4:1 (2014), 26–33.
87. Chou, H.S., Hsieh, C.C., Charles, R., Wang, L., Wagner, T., Fung, J.J., Qian, S., Lu, L.L., Myeloid-derived suppressor cells protect islet transplants by B7-H1 mediated enhancement of T regulatory cells. Transplantation 93:3 (2012), 272–282.
88. Chou, H.S., Hsieh, C.C., Yang, H.R., Wang, L., Arakawa, Y., Brown, K., Wu, Q., Lin, F., Peters, M., Fung, J.J., Lu, L., Qian, S., Hepatic stellate cells regulate immune response by way of induction of myeloid suppressor cells in mice. Hepatology 53:3 (2011), 1007–1019.
89. Haile, L.A., von Wasielewski, R., Gamrekelashvili, J., Kruger, C., Bachmann, O., Westendorf, A.M., Buer, J., Liblau, R., Manns, M.P., Korangy, F., Greten, T.F., Myeloid-derived suppressor cells in inflammatory bowel disease: a new immunoregulatory pathway. Gastroenterology 135:3 (2008), 871–881 881 e1–5.
90. Fujii, W., Ashihara, E., Hirai, H., Nagahara, H., Kajitani, N., Fujioka, K., Murakami, K., Seno, T., Yamamoto, A., Ishino, H., Kohno, M., Maekawa, T., Kawahito, Y., Myeloid-derived suppressor cells play crucial roles in the regulation of mouse collagen-induced arthritis. J. Immunol. 191:3 (2013), 1073–1081.
91. Crook, K.R., Jin, M., Weeks, M.F., Rampersad, R.R., Baldi, R.M., Glekas, A.S., Shen, Y., Esserman, D.A., Little, P., Schwartz, T.A., Liu, P., Myeloid-derived suppressor cells regulate T cell and B cell responses during autoimmune disease. J. Leukoc. Biol. 97:3 (2015), 573–582.
92. Guan, Q., Moreno, S., Qing, G., Weiss, C.R., Lu, L., Bernstein, C.N., Warrington, R.J., Ma, Y., Peng, Z., The role and potential therapeutic application of myeloid-derived suppressor cells in TNBS-induced colitis. J. Leukoc. Biol. 94:4 (2013), 803–811.
93. Zhang, R., Ito, S., Nishio, N., Cheng, Z., Suzuki, H., Isobe, K.I., Dextran sulphate sodium increases splenic Gr1(+)CD11b(+) cells which accelerate recovery from colitis following intravenous transplantation. Clin. Exp. Immunol. 164:3 (2011), 417–427.
94. Tu, Z., Li, Y., Smith, D., Doller, C., Sugita, S., Chan, C.C., Qian, S., Fung, J., Caspi, R.R., Lu, L., Lin, F., Myeloid suppressor cells induced by retinal pigment epithelial cells inhibit autoreactive T-cell responses that lead to experimental autoimmune uveitis. Investig. Ophthalmol. Vis. Sci. 53:2 (2012), 959–966.
95. Wegner, A., Verhagen, J., Wraith, D.C., Myeloid-derived suppressor cells mediate tolerance induction in autoimmune disease. Immunology 151:1 (2017), 26–42.
96. Andersen, M.H., Cancer and autoimmunity. Semin. Immunopathol. 39:3 (2017), 241–243.
97. Khan, I.S., Mouchess, M.L., Zhu, M.L., Conley, B., Fasano, K.J., Hou, Y., Fong, L., Su, M.A., Anderson, M.S., Enhancement of an anti-tumor immune response by transient blockade of central T cell tolerance. J. Exp. Med. 211:5 (2014), 761–768.
98. Bottazzi, B., Polentarutti, N., Acero, R., Balsari, A., Boraschi, D., Ghezzi, P., Salmona, M., Mantovani, A., Regulation of the macrophage content of neoplasms by chemoattractants. Science 220:4593 (1983), 210–212.
99. Suzuki, E., Kapoor, V., Jassar, A.S., Kaiser, L.R., Albelda, S.M., Gemcitabine selectively eliminates splenic Gr-1+/CD11b+ myeloid suppressor cells in tumor-bearing animals and enhances antitumor immune activity. Clin. Cancer Res. 11:18 (2005), 6713–6721.
100. Vincent, J., Mignot, G., Chalmin, F., Ladoire, S., Bruchard, M., Chevriaux, A., Martin, F., Apetoh, L., Rebe, C., Ghiringhelli, F., 5-Fluorouracil selectively kills tumor-associated myeloid-derived suppressor cells resulting in enhanced T cell-dependent antitumor immunity. Cancer Res. 70:8 (2010), 3052–3061.
101. Taylor, P.C., Feldmann, M., Anti-TNF biologic agents: still the therapy of choice for rheumatoid arthritis. Nat. Rev. Rheumatol. 5:10 (2009), 578–582.
102. Gerspach, J., Pfizenmaier, K., Wajant, H., Improving TNF as a cancer therapeutic: tailor-made TNF fusion proteins with conserved antitumor activity and reduced systemic side effects. Biofactors 35:4 (2009), 364–372.
103. Vacchelli, E., Galluzzi, L., Eggermont, A., Galon, J., Tartour, E., Zitvogel, L., Kroemer, G., Trial watch: immunostimulatory cytokines. Oncoimmunology 1:4 (2012), 493–506.
104. Pitt, J.M., Vetizou, M., Daillere, R., Roberti, M.P., Yamazaki, T., Routy, B., Lepage, P., Boneca, I.G., Chamaillard, M., Kroemer, G., Zitvogel, L., Resistance mechanisms to immune-checkpoint blockade in cancer: tumor-intrinsic and -extrinsic factors. Immunity 44:6 (2016), 1255–1269.
105. Gnerlich, J.L., Mitchem, J.B., Weir, J.S., Sankpal, N.V., Kashiwagi, H., Belt, B.A., Porembka, M.R., Herndon, J.M., Eberlein, T.J., Goedegebuure, P., Linehan, D.C., Induction of Th17 cells in the tumor microenvironment improves survival in a murine model of pancreatic cancer. J. Immunol. 185:7 (2010), 4063–4071.
106. Kesselring, R., Thiel, A., Pries, R., Trenkle, T., Wollenberg, B., Human Th17 cells can be induced through head and neck cancer and have a functional impact on HNSCC development. Br. J. Cancer 103:8 (2010), 1245–1254.
107. Lan, C., Huang, X., Lin, S., Huang, H., Cai, Q., Lu, J., Liu, J., High density of IL-17-producing cells is associated with improved prognosis for advanced epithelial ovarian cancer. Cell Tissue Res. 352:2 (2013), 351–359.