Origin and Role of a Subset of Tumor-Associated Neutrophils with Antigen-Presenting Cell Features in Early-Stage Human Lung Cancer

Cancer Cell

Volumn 30, Issue 1, 2016, Pages 120-135

  Singhal, Sunil ^a,c   Bhojnagarwala, Pratik S ^a   O'Brien, Shaun ^a   Moon, Edmund K ^a   Garfall, Alfred L ^b   Rao, Abhishek S ^a   Quatromoni, Jon G ^a   Stephen, Tom Li ^d   Litzky, Leslie ^a   Deshpande, Charuhas ^a   Feldman, Michael D ^a   Hancock, Wayne W ^a,e   Conejo Garcia, Jose R ^d   Albelda, Steven M ^a   Eruslanov, Evgeniy B ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

^c VETERANS AFFAIRS MEDICAL CENTER   (United States)

^d WISTAR INSTITUTE   (United States)

^e CHILDREN S HOSPITAL OF PHILADELPHIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD11B ANTIGEN; CD15 ANTIGEN; CD16 ANTIGEN; COMMON ACUTE LYMPHOBLASTIC LEUKEMIA ANTIGEN; GAMMA INTERFERON; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; IKAROS TRANSCRIPTION FACTOR;

ANTIGEN PRESENTATION; ANTIGEN PRESENTING CELL; ARTICLE; CANCER STAGING; CELL SUBPOPULATION; CELLULAR IMMUNITY; CONTROLLED STUDY; EARLY CANCER; GRANULOCYTE; HUMAN; HUMAN CELL; LUNG CANCER; PRIORITY JOURNAL; STEM CELL; TUMOR ASSOCIATED LEUKOCYTE; TUMOR IMMUNITY; TUMOR MICROENVIRONMENT; CYTOLOGY; CYTOTOXIC T LYMPHOCYTE; GENE EXPRESSION REGULATION; IMMUNOLOGY; LUNG TUMOR; METABOLISM; NEUTROPHIL;

ANTIGEN-PRESENTING CELLS; GENE EXPRESSION REGULATION, NEOPLASTIC; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HUMANS; IKAROS TRANSCRIPTION FACTOR; INTERFERON-GAMMA; LUNG NEOPLASMS; NEOPLASM STAGING; NEUTROPHILS; T-LYMPHOCYTES, CYTOTOXIC;

EID: 84978371387     PISSN: 15356108     EISSN: 18783686     Source Type: Journal    
DOI: 10.1016/j.ccell.2016.06.001     Document Type: Article

References (38)

1. Abi Abdallah, D.S., Egan, C.E., Butcher, B.A., Denkers, E.Y., Mouse neutrophils are professional antigen-presenting cells programmed to instruct Th1 and Th17 T-cell differentiation. Int. Immunol. 5 (2011), 317–326.
2. Araki, H., Katayama, N., Yamashita, Y., Mano, H., Fujieda, A., Usui, E., Mitani, H., Ohishi, K., Nishii, K., Masuya, M., et al. Reprogramming of human postmitotic neutrophils into macrophages by growth factors. Blood 8 (2004), 2973–2980.
3. Ashtekar, A.R., Saha, B., Poly's plea: membership to the club of APCs. Trends Immunol. 9 (2003), 485–490.
4. Brandau, S., The dichotomy of neutrophil granulocytes in cancer. Semin. Cancer Biol. 3 (2013), 139–140.
5. Carus, A., Ladekarl, M., Hager, H., Pilegaard, H., Nielsen, P.S., Donskov, F., Tumor-associated neutrophils and macrophages in non-small cell lung cancer: no immediate impact on patient outcome. Lung Cancer 1 (2013), 130–137.
6. Dai, Z.J., Gao, J., Ma, X.B., Yan, K., Liu, X.X., Kang, H.F., Ji, Z.Z., Guan, H.T., Wang, X.J., Up-regulation of hypoxia inducible factor-1alpha by cobalt chloride correlates with proliferation and apoptosis in PC-2 cells. J. Exp. Clin. Cancer Res., 31, 2012, 28.
7. Dallegri, F., Ottonello, L., Neutrophil-mediated cytotoxicity against tumour cells: state of art. Arch. Immunol. Ther. Exp. (Warsz) 1 (1992), 39–42.
8. Dumortier, A., Kirstetter, P., Kastner, P., Chan, S., Ikaros regulates neutrophil differentiation. Blood 6 (2003), 2219–2226.
9. Elghetany, M.T., Surface antigen changes during normal neutrophilic development: a critical review. Blood Cells Mol. Dis. 2 (2002), 260–274.
10. Eruslanov, E.B., Bhojnagarwala, P.S., Quatromoni, J.G., Stephen, T.L., Ranganathan, A., Deshpande, C., Akimova, T., Vachani, A., Litzky, L., Hancock, W.W., et al. Tumor-associated neutrophils stimulate T cell responses in early-stage human lung cancer. J. Clin. Invest. 12 (2014), 5466–5480.
11. Fridlender, Z.G., Sun, J., Kim, S., Kapoor, V., Cheng, G., Ling, L., Worthen, G.S., Albelda, S.M., Polarization of tumor-associated neutrophil phenotype by TGF-beta: “N1” versus “N2” TAN. Cancer Cell 3 (2009), 183–194.
12. Geng, S., Matsushima, H., Okamoto, T., Yao, Y., Lu, R., Page, K., Blumenthal, R.M., Ward, N.L., Miyazaki, T., Takashima, A., Emergence, origin, and function of neutrophil-dendritic cell hybrids in experimentally induced inflammatory lesions in mice. Blood 10 (2013), 1690–1700.
13. Gosselin, E.J., Wardwell, K., Rigby, W.F., Guyre, P.M., Induction of MHC class II on human polymorphonuclear neutrophils by granulocyte/macrophage colony-stimulating factor, IFN-gamma, and IL-3. J. Immunol. 3 (1993), 1482–1490.
14. Granot, Z., Fridlender, Z.G., Plasticity beyond cancer cells and the “immunosuppressive switch”. Cancer Res. 21 (2015), 4441–4445.
15. Grivennikov, S.I., Greten, F.R., Karin, M., Immunity, inflammation, and cancer. Cell 6 (2010), 883–899.
16. Houghton, A.M., The paradox of tumor-associated neutrophils: fueling tumor growth with cytotoxic substances. Cell Cycle 9 (2010), 1732–1737.
17. Iking-Konert, C., Cseko, C., Wagner, C., Stegmaier, S., Andrassy, K., Hansch, G.M., Transdifferentiation of polymorphonuclear neutrophils: acquisition of CD83 and other functional characteristics of dendritic cells. J. Mol. Med. (Berl.) 8 (2001), 464–474.
18. Iking-Konert, C., Ostendorf, B., Sander, O., Jost, M., Wagner, C., Joosten, L., Schneider, M., Hansch, G.M., Transdifferentiation of polymorphonuclear neutrophils to dendritic-like cells at the site of inflammation in rheumatoid arthritis: evidence for activation by T cells. Ann. Rheum. Dis. 10 (2005), 1436–1442.
19. Ilie, M., Hofman, V., Ortholan, C., Bonnetaud, C., Coelle, C., Mouroux, J., Hofman, P., Predictive clinical outcome of the intratumoral CD66b-positive neutrophil-to-CD8-positive T-cell ratio in patients with resectable nonsmall cell lung cancer. Cancer 6 (2012), 1726–1737.
20. Koffel, R., Meshcheryakova, A., Warszawska, J., Hennig, A., Wagner, K., Jorgl, A., Gubi, D., Moser, D., Hladik, A., Hoffmann, U., et al. Monocytic cell differentiation from band-stage neutrophils under inflammatory conditions via MKK6 activation. Blood 17 (2014), 2713–2724.
21. Kronke, J., Hurst, S.N., Ebert, B.L., Lenalidomide induces degradation of IKZF1 and IKZF3. Oncoimmunology, 7, 2014, e941742.
22. Mantovani, A., Cassatella, M.A., Costantini, C., Jaillon, S., Neutrophils in the activation and regulation of innate and adaptive immunity. Nat. Rev. Immunol. 8 (2011), 519–531.
23. Matsushima, H., Geng, S., Lu, R., Okamoto, T., Yao, Y., Mayuzumi, N., Kotol, P.F., Chojnacki, B.J., Miyazaki, T., Gallo, R.L., Takashima, A., Neutrophil differentiation into a unique hybrid population exhibiting dual phenotype and functionality of neutrophils and dendritic cells. Blood 10 (2013), 1677–1689.
24. Moon, E.K., Ranganathan, R., Eruslanov, E., Kim, S., Newick, K., O'Brien, S., Lo, A., Liu, X., Zhao, Y., Albelda, S.M., Blockade of programmed death 1 augments the ability of human T cells engineered to target NY-ESO-1 to control tumor growth after adoptive transfer. Clin. Cancer Res. 22 (2016), 436–447.
25. Nagata, Y., Ono, S., Matsuo, M., Gnjatic, S., Valmori, D., Ritter, G., Garrett, W., Old, L.J., Mellman, I., Differential presentation of a soluble exogenous tumor antigen, NY-ESO-1, by distinct human dendritic cell populations. Proc. Natl. Acad. Sci. USA 16 (2002), 10629–10634.
26. O'Brien, S., Thomas, R.M., Wertheim, G.B., Zhang, F., Shen, H., Wells, A.D., Ikaros imposes a barrier to CD8+ T cell differentiation by restricting autocrine IL-2 production. J. Immunol. 11 (2014), 5118–5129.
27. Oehler, L., Majdic, O., Pickl, W.F., Stockl, J., Riedl, E., Drach, J., Rappersberger, K., Geissler, K., Knapp, W., Neutrophil granulocyte-committed cells can be driven to acquire dendritic cell characteristics. J. Exp. Med. 7 (1998), 1019–1028.
28. Papathanasiou, P., Perkins, A.C., Cobb, B.S., Ferrini, R., Sridharan, R., Hoyne, G.F., Nelms, K.A., Smale, S.T., Goodnow, C.C., Widespread failure of hematolymphoid differentiation caused by a recessive niche-filling allele of the Ikaros transcription factor. Immunity 1 (2003), 131–144.
29. Piccard, H., Muschel, R.J., Opdenakker, G., On the dual roles and polarized phenotypes of neutrophils in tumor development and progression. Crit. Rev. Oncol. Hematol. 3 (2012), 296–309.
30. Potter, N.S., Harding, C.V., Neutrophils process exogenous bacteria via an alternate class I MHC processing pathway for presentation of peptides to T lymphocytes. J. Immunol. 5 (2001), 2538–2546.
31. Quatromoni, J.G., Singhal, S., Bhojnagarwala, P., Hancock, W.W., Albelda, S.M., Eruslanov, E., An optimized disaggregation method for human lung tumors that preserves the phenotype and function of the immune cells. J. Leukoc. Biol. 1 (2015), 201–209.
32. Radsak, M., Iking-Konert, C., Stegmaier, S., Andrassy, K., Hansch, G.M., Polymorphonuclear neutrophils as accessory cells for T-cell activation: major histocompatibility complex class II restricted antigen-dependent induction of T-cell proliferation. Immunology 4 (2000), 521–530.
33. Reinisch, W., Tillinger, W., Lichtenberger, C., Gangl, A., Willheim, M., Scheiner, O., Steger, G., In vivo induction of HLA-DR on human neutrophils in patients treated with interferon-gamma. Blood, 7, 1996, 3068.
34. Schreiber, R.D., Old, L.J., Smyth, M.J., Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion. Science 6024 (2011), 1565–1570.
35. Tvinnereim, A.R., Hamilton, S.E., Harty, J.T., Neutrophil involvement in cross-priming CD8+ T cell responses to bacterial antigens. J. Immunol. 3 (2004), 1994–2002.
36. van Egmond, M., Bakema, J.E., Neutrophils as effector cells for antibody-based immunotherapy of cancer. Semin. Cancer Biol. 3 (2013), 190–199.
37. Wagner, C., Iking-Konert, C., Hug, F., Stegmaier, S., Heppert, V., Wentzensen, A., Hansch, G.M., Cellular inflammatory response to persistent localized Staphylococcus aureus infection: phenotypical and functional characterization of polymorphonuclear neutrophils (PMN). Clin. Exp. Immunol. 1 (2006), 70–77.
38. Yanez, A., Ng, M.Y., Hassanzadeh-Kiabi, N., Goodridge, H.S., IRF8 acts in lineage-committed rather than oligopotent progenitors to control neutrophil vs monocyte production. Blood 9 (2015), 1452–1459.