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Published in: Seminars in Immunopathology 2/2013

01-03-2013 | Review

Protumor and antitumor functions of neutrophil granulocytes

Authors: Sven Brandau, Claudia A. Dumitru, Stephan Lang

Published in: Seminars in Immunopathology | Issue 2/2013

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Abstract

Neutrophils are primary inflammatory cells and absolutely essential to protect the host during the early phases of microbial infection. Their role in cancer is less clear. Current evidence suggests that neutrophils show high functional plasticity and can adopt protumor and antitumor activity. Protumor neutrophils are functionally related to the recently described granulocytic myeloid-derived suppressor cells. We propose a model in which homeostatic chronic recruitment and activation of neutrophils result in mainly protumor activity. In contrast, therapeutic interventions in many cases elicit acute activation, enhance direct effector functions as well as indirect regulatory functions of neutrophils with potent antitumor activity. Conversion of protumor activity of neutrophils into antitumor activity by means of appropriate stimulation or modulation may offer new possibilities in biologic therapy of cancer.
Literature
1.
go back to reference Schreiber RD, Old LJ, Smyth MJ (2011) Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion. Science 331:1565–1570PubMedCrossRef Schreiber RD, Old LJ, Smyth MJ (2011) Cancer immunoediting: integrating immunity’s roles in cancer suppression and promotion. Science 331:1565–1570PubMedCrossRef
2.
go back to reference Faurschou M, Borregaard N (2003) Neutrophil granules and secretory vesicles in inflammation. Microbes Infect 5:1317–1327PubMedCrossRef Faurschou M, Borregaard N (2003) Neutrophil granules and secretory vesicles in inflammation. Microbes Infect 5:1317–1327PubMedCrossRef
3.
go back to reference Nathan C (2006) Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol 6:173–182PubMedCrossRef Nathan C (2006) Neutrophils and immunity: challenges and opportunities. Nat Rev Immunol 6:173–182PubMedCrossRef
4.
5.
go back to reference Borregaard N, Sorensen OE, Theilgaard-Monch K (2007) Neutrophil granules: a library of innate immunity proteins. Trends Immunol 28:340–345PubMedCrossRef Borregaard N, Sorensen OE, Theilgaard-Monch K (2007) Neutrophil granules: a library of innate immunity proteins. Trends Immunol 28:340–345PubMedCrossRef
6.
go back to reference Halazun KJ, Hardy MA, Rana AA, Woodland DC, Luyten EJ, Mahadev S, Witkowski P, Siegel AB, Brown RS Jr, Emond JC (2009) Negative impact of neutrophil-lymphocyte ratio on outcome after liver transplantation for hepatocellular carcinoma. Ann Surg 250:141–151PubMedCrossRef Halazun KJ, Hardy MA, Rana AA, Woodland DC, Luyten EJ, Mahadev S, Witkowski P, Siegel AB, Brown RS Jr, Emond JC (2009) Negative impact of neutrophil-lymphocyte ratio on outcome after liver transplantation for hepatocellular carcinoma. Ann Surg 250:141–151PubMedCrossRef
7.
go back to reference He JR, Shen GP, Ren ZF, Qin H, Cui C, Zhang Y, Zeng YX, Jia WH (2012) Pretreatment levels of peripheral neutrophils and lymphocytes as independent prognostic factors in patients with nasopharyngeal carcinoma. Head Neck. doi:10.1002/hed.22008 [Epub ahead of print] He JR, Shen GP, Ren ZF, Qin H, Cui C, Zhang Y, Zeng YX, Jia WH (2012) Pretreatment levels of peripheral neutrophils and lymphocytes as independent prognostic factors in patients with nasopharyngeal carcinoma. Head Neck. doi:10.​1002/​hed.​22008 [Epub ahead of print]
8.
go back to reference Jensen HK, Donskov F, Marcussen N, Nordsmark M, Lundbeck F, von der Maase H (2009) Presence of intratumoral neutrophils is an independent prognostic factor in localized renal cell carcinoma. J Clin Oncol 27:4709–4717PubMedCrossRef Jensen HK, Donskov F, Marcussen N, Nordsmark M, Lundbeck F, von der Maase H (2009) Presence of intratumoral neutrophils is an independent prognostic factor in localized renal cell carcinoma. J Clin Oncol 27:4709–4717PubMedCrossRef
9.
go back to reference Schmidt H, Bastholt L, Geertsen P, Christensen IJ, Larsen S, Gehl J, von der Maase H (2005) Elevated neutrophil and monocyte counts in peripheral blood are associated with poor survival in patients with metastatic melanoma: a prognostic model. Br J Cancer 93:273–278PubMedCrossRef Schmidt H, Bastholt L, Geertsen P, Christensen IJ, Larsen S, Gehl J, von der Maase H (2005) Elevated neutrophil and monocyte counts in peripheral blood are associated with poor survival in patients with metastatic melanoma: a prognostic model. Br J Cancer 93:273–278PubMedCrossRef
10.
go back to reference Walsh SR, Cook EJ, Goulder F, Justin TA, Keeling NJ (2005) Neutrophil-lymphocyte ratio as a prognostic factor in colorectal cancer. J Surg Oncol 91:181–184PubMedCrossRef Walsh SR, Cook EJ, Goulder F, Justin TA, Keeling NJ (2005) Neutrophil-lymphocyte ratio as a prognostic factor in colorectal cancer. J Surg Oncol 91:181–184PubMedCrossRef
11.
go back to reference Dumitru CA, Moses K, Trellakis S, Lang S, Brandau S (2012) Neutrophils and granulocytic myeloid-derived suppressor cells: immunophenotyping, cell biology and clinical relevance in human oncology. Cancer Immunol Immunother 61(8):1155–1167PubMedCrossRef Dumitru CA, Moses K, Trellakis S, Lang S, Brandau S (2012) Neutrophils and granulocytic myeloid-derived suppressor cells: immunophenotyping, cell biology and clinical relevance in human oncology. Cancer Immunol Immunother 61(8):1155–1167PubMedCrossRef
12.
go back to reference Almand B, Clark JI, Nikitina E, van Beynen J, English NR, Knight SC, Carbone DP, Gabrilovich DI (2001) Increased production of immature myeloid cells in cancer patients: a mechanism of immunosuppression in cancer. J Immunol 166:678–689PubMed Almand B, Clark JI, Nikitina E, van Beynen J, English NR, Knight SC, Carbone DP, Gabrilovich DI (2001) Increased production of immature myeloid cells in cancer patients: a mechanism of immunosuppression in cancer. J Immunol 166:678–689PubMed
13.
go back to reference Trellakis S, Farjah H, Bruderek K, Dumitru CA, Hoffmann TK, Lang S, Brandau S (2011) Peripheral blood neutrophil granulocytes from patients with head and neck squamous cell carcinoma functionally differ from their counterparts in healthy donors. Int J Immunopathol Pharmacol 24:683–693PubMed Trellakis S, Farjah H, Bruderek K, Dumitru CA, Hoffmann TK, Lang S, Brandau S (2011) Peripheral blood neutrophil granulocytes from patients with head and neck squamous cell carcinoma functionally differ from their counterparts in healthy donors. Int J Immunopathol Pharmacol 24:683–693PubMed
14.
go back to reference Brandau S, Trellakis S, Bruderek K, Schmaltz D, Steller G, Elian M, Suttmann H, Schenck M, Welling J, Zabel P, Lang S (2011) Myeloid-derived suppressor cells in the peripheral blood of cancer patients contain a subset of immature neutrophils with impaired migratory properties. J Leukoc Biol 89:311–317PubMedCrossRef Brandau S, Trellakis S, Bruderek K, Schmaltz D, Steller G, Elian M, Suttmann H, Schenck M, Welling J, Zabel P, Lang S (2011) Myeloid-derived suppressor cells in the peripheral blood of cancer patients contain a subset of immature neutrophils with impaired migratory properties. J Leukoc Biol 89:311–317PubMedCrossRef
15.
go back to reference Choi J, Suh B, Ahn YO, Kim TM, Lee JO, Lee SH, Heo DS (2012) CD15+/CD16low human granulocytes from terminal cancer patients: granulocytic myeloid-derived suppressor cells that have suppressive function. Tumour Biol 33:121–129PubMedCrossRef Choi J, Suh B, Ahn YO, Kim TM, Lee JO, Lee SH, Heo DS (2012) CD15+/CD16low human granulocytes from terminal cancer patients: granulocytic myeloid-derived suppressor cells that have suppressive function. Tumour Biol 33:121–129PubMedCrossRef
16.
go back to reference Cortez-Retamozo V, Etzrodt M, Newton A, Rauch PJ, Chudnovskiy A, Berger C, Ryan RJ, Iwamoto Y, Marinelli B, Gorbatov R, Forghani R, Novobrantseva TI, Koteliansky V, Figueiredo JL, Chen JW, Anderson DG, Nahrendorf M, Swirski FK, Weissleder R, Pittet MJ (2012) Origins of tumor-associated macrophages and neutrophils. Proc Natl Acad Sci U S A 109:2491–2496PubMedCrossRef Cortez-Retamozo V, Etzrodt M, Newton A, Rauch PJ, Chudnovskiy A, Berger C, Ryan RJ, Iwamoto Y, Marinelli B, Gorbatov R, Forghani R, Novobrantseva TI, Koteliansky V, Figueiredo JL, Chen JW, Anderson DG, Nahrendorf M, Swirski FK, Weissleder R, Pittet MJ (2012) Origins of tumor-associated macrophages and neutrophils. Proc Natl Acad Sci U S A 109:2491–2496PubMedCrossRef
17.
go back to reference Gabrilovich DI, Velders MP, Sotomayor EM, Kast WM (2001) Mechanism of immune dysfunction in cancer mediated by immature Gr-1+ myeloid cells. J Immunol 166:5398–5406PubMed Gabrilovich DI, Velders MP, Sotomayor EM, Kast WM (2001) Mechanism of immune dysfunction in cancer mediated by immature Gr-1+ myeloid cells. J Immunol 166:5398–5406PubMed
18.
go back to reference Youn JI, Gabrilovich DI (2010) The biology of myeloid-derived suppressor cells: the blessing and the curse of morphological and functional heterogeneity. Eur J Immunol 40:2969–2975PubMedCrossRef Youn JI, Gabrilovich DI (2010) The biology of myeloid-derived suppressor cells: the blessing and the curse of morphological and functional heterogeneity. Eur J Immunol 40:2969–2975PubMedCrossRef
19.
go back to reference Gabrilovich DI, Bronte V, Chen SH, Colombo MP, Ochoa A, Ostrand-Rosenberg S, Schreiber H (2007) The terminology issue for myeloid-derived suppressor cells. Cancer Res 67:425PubMedCrossRef Gabrilovich DI, Bronte V, Chen SH, Colombo MP, Ochoa A, Ostrand-Rosenberg S, Schreiber H (2007) The terminology issue for myeloid-derived suppressor cells. Cancer Res 67:425PubMedCrossRef
20.
go back to reference Montero AJ, Diaz-Montero CM, Kyriakopoulos CE, Bronte V, Mandruzzato S (2012) Myeloid-derived suppressor cells in cancer patients: a clinical perspective. J Immunother 35:107–115PubMedCrossRef Montero AJ, Diaz-Montero CM, Kyriakopoulos CE, Bronte V, Mandruzzato S (2012) Myeloid-derived suppressor cells in cancer patients: a clinical perspective. J Immunother 35:107–115PubMedCrossRef
21.
go back to reference Nagaraj S, Gabrilovich DI (2010) Myeloid-derived suppressor cells in human cancer. Cancer J 16:348–353PubMedCrossRef Nagaraj S, Gabrilovich DI (2010) Myeloid-derived suppressor cells in human cancer. Cancer J 16:348–353PubMedCrossRef
22.
go back to reference Ostrand-Rosenberg S, Sinha P (2009) Myeloid-derived suppressor cells: linking inflammation and cancer. J Immunol 182:4499–4506PubMedCrossRef Ostrand-Rosenberg S, Sinha P (2009) Myeloid-derived suppressor cells: linking inflammation and cancer. J Immunol 182:4499–4506PubMedCrossRef
23.
go back to reference Youn JI, Collazo M, Shalova IN, Biswas SK, Gabrilovich DI (2012) Characterization of the nature of granulocytic myeloid-derived suppressor cells in tumor-bearing mice. J Leukoc Biol 91:167–181PubMedCrossRef Youn JI, Collazo M, Shalova IN, Biswas SK, Gabrilovich DI (2012) Characterization of the nature of granulocytic myeloid-derived suppressor cells in tumor-bearing mice. J Leukoc Biol 91:167–181PubMedCrossRef
24.
go back to reference Fridlender ZG, Sun J, Mishalian I, Singhal S, Cheng G, Kapoor V, Horng W, Fridlender G, Bayuh R, Worthen GS, Albelda SM (2012) Transcriptomic analysis comparing tumor-associated neutrophils with granulocytic myeloid-derived suppressor cells and normal neutrophils. PLoS One 7:e31524PubMedCrossRef Fridlender ZG, Sun J, Mishalian I, Singhal S, Cheng G, Kapoor V, Horng W, Fridlender G, Bayuh R, Worthen GS, Albelda SM (2012) Transcriptomic analysis comparing tumor-associated neutrophils with granulocytic myeloid-derived suppressor cells and normal neutrophils. PLoS One 7:e31524PubMedCrossRef
25.
go back to reference Ribechini E, Greifenberg V, Sandwick S, Lutz MB (2010) Subsets, expansion and activation of myeloid-derived suppressor cells. Med Microbiol Immunol 199:273–281PubMedCrossRef Ribechini E, Greifenberg V, Sandwick S, Lutz MB (2010) Subsets, expansion and activation of myeloid-derived suppressor cells. Med Microbiol Immunol 199:273–281PubMedCrossRef
26.
go back to reference Condamine T, Gabrilovich DI (2011) Molecular mechanisms regulating myeloid-derived suppressor cell differentiation and function. Trends Immunol 32:19–25PubMedCrossRef Condamine T, Gabrilovich DI (2011) Molecular mechanisms regulating myeloid-derived suppressor cell differentiation and function. Trends Immunol 32:19–25PubMedCrossRef
27.
go back to reference Gabrilovich DI, Ostrand-Rosenberg S, Bronte V (2012) Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol 12:253–268PubMedCrossRef Gabrilovich DI, Ostrand-Rosenberg S, Bronte V (2012) Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol 12:253–268PubMedCrossRef
28.
go back to reference Basu S, Dunn A, Ward A (2002) G-CSF: function and modes of action (Review). Int J Mol Med 10:3–10PubMed Basu S, Dunn A, Ward A (2002) G-CSF: function and modes of action (Review). Int J Mol Med 10:3–10PubMed
29.
go back to reference Waight JD, Hu Q, Miller A, Liu S, Abrams SI (2011) Tumor-derived G-CSF facilitates neoplastic growth through a granulocytic myeloid-derived suppressor cell-dependent mechanism. PLoS One 6:e27690PubMedCrossRef Waight JD, Hu Q, Miller A, Liu S, Abrams SI (2011) Tumor-derived G-CSF facilitates neoplastic growth through a granulocytic myeloid-derived suppressor cell-dependent mechanism. PLoS One 6:e27690PubMedCrossRef
30.
go back to reference Roberts AW (2005) G-CSF: a key regulator of neutrophil production, but that’s not all! Growth Factors 23:33–41PubMedCrossRef Roberts AW (2005) G-CSF: a key regulator of neutrophil production, but that’s not all! Growth Factors 23:33–41PubMedCrossRef
31.
go back to reference Berliner N, Hsing A, Graubert T, Sigurdsson F, Zain M, Bruno E, Hoffman R (1995) Granulocyte colony-stimulating factor induction of normal human bone marrow progenitors results in neutrophil-specific gene expression. Blood 85:799–803PubMed Berliner N, Hsing A, Graubert T, Sigurdsson F, Zain M, Bruno E, Hoffman R (1995) Granulocyte colony-stimulating factor induction of normal human bone marrow progenitors results in neutrophil-specific gene expression. Blood 85:799–803PubMed
32.
go back to reference Lechner MG, Liebertz DJ, Epstein AL (2010) Characterization of cytokine-induced myeloid-derived suppressor cells from normal human peripheral blood mononuclear cells. J Immunol 185:2273–2284PubMedCrossRef Lechner MG, Liebertz DJ, Epstein AL (2010) Characterization of cytokine-induced myeloid-derived suppressor cells from normal human peripheral blood mononuclear cells. J Immunol 185:2273–2284PubMedCrossRef
33.
go back to reference Solito S, Falisi E, Diaz-Montero CM, Doni A, Pinton L, Rosato A, Francescato S, Basso G, Zanovello P, Onicescu G, Garrett-Mayer E, Montero AJ, Bronte V, Mandruzzato S (2011) A human promyelocytic-like population is responsible for the immune suppression mediated by myeloid-derived suppressor cells. Blood 118:2254–2265PubMedCrossRef Solito S, Falisi E, Diaz-Montero CM, Doni A, Pinton L, Rosato A, Francescato S, Basso G, Zanovello P, Onicescu G, Garrett-Mayer E, Montero AJ, Bronte V, Mandruzzato S (2011) A human promyelocytic-like population is responsible for the immune suppression mediated by myeloid-derived suppressor cells. Blood 118:2254–2265PubMedCrossRef
34.
go back to reference Joshita S, Nakazawa K, Sugiyama Y, Kamijo A, Matsubayashi K, Miyabayashi H, Furuta K, Kitano K, Kawa S (2009) Granulocyte-colony stimulating factor-producing pancreatic adenosquamous carcinoma showing aggressive clinical course. Intern Med 48:687–691PubMedCrossRef Joshita S, Nakazawa K, Sugiyama Y, Kamijo A, Matsubayashi K, Miyabayashi H, Furuta K, Kitano K, Kawa S (2009) Granulocyte-colony stimulating factor-producing pancreatic adenosquamous carcinoma showing aggressive clinical course. Intern Med 48:687–691PubMedCrossRef
35.
go back to reference Nakada T, Sato H, Inoue F, Mizorogi F, Nagayama K, Tanaka T (1996) The production of colony-stimulating factors by thyroid carcinoma is associated with marked neutrophilia and eosinophilia. Intern Med 35:815–820PubMedCrossRef Nakada T, Sato H, Inoue F, Mizorogi F, Nagayama K, Tanaka T (1996) The production of colony-stimulating factors by thyroid carcinoma is associated with marked neutrophilia and eosinophilia. Intern Med 35:815–820PubMedCrossRef
36.
go back to reference Matsumoto Y, Mabuchi S, Muraji M, Morii E, Kimura T (2010) Squamous cell carcinoma of the uterine cervix producing granulocyte colony-stimulating factor: a report of 4 cases and a review of the literature. Int J Gynecol Cancer 20:417–421PubMedCrossRef Matsumoto Y, Mabuchi S, Muraji M, Morii E, Kimura T (2010) Squamous cell carcinoma of the uterine cervix producing granulocyte colony-stimulating factor: a report of 4 cases and a review of the literature. Int J Gynecol Cancer 20:417–421PubMedCrossRef
37.
go back to reference Corzo CA, Condamine T, Lu L, Cotter MJ, Youn JI, Cheng P, Cho HI, Celis E, Quiceno DG, Padhya T, McCaffrey TV, McCaffrey JC, Gabrilovich DI (2010) HIF-1alpha regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J Exp Med 207:2439–2453PubMedCrossRef Corzo CA, Condamine T, Lu L, Cotter MJ, Youn JI, Cheng P, Cho HI, Celis E, Quiceno DG, Padhya T, McCaffrey TV, McCaffrey JC, Gabrilovich DI (2010) HIF-1alpha regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment. J Exp Med 207:2439–2453PubMedCrossRef
39.
go back to reference Lazennec G, Richmond A (2010) Chemokines and chemokine receptors: new insights into cancer-related inflammation. Trends Mol Med 16:133–144PubMedCrossRef Lazennec G, Richmond A (2010) Chemokines and chemokine receptors: new insights into cancer-related inflammation. Trends Mol Med 16:133–144PubMedCrossRef
40.
go back to reference Hannelien V, Karel G, Jo VD, Sofie S (2012) The role of CXC chemokines in the transition of chronic inflammation to esophageal and gastric cancer. Biochim Biophys Acta 1825:117–129PubMed Hannelien V, Karel G, Jo VD, Sofie S (2012) The role of CXC chemokines in the transition of chronic inflammation to esophageal and gastric cancer. Biochim Biophys Acta 1825:117–129PubMed
41.
42.
go back to reference Zhou SL, Dai Z, Zhou ZJ, Wang XY, Yang GH, Wang Z, Huang XW, Fan J, Zhou J (2012) Overexpression of CXCL5 mediates neutrophil infiltration and indicates poor prognosis for hepatocellular carcinoma. Hepatology. doi:10.1002/hep.25907 [Epub ahead of print] Zhou SL, Dai Z, Zhou ZJ, Wang XY, Yang GH, Wang Z, Huang XW, Fan J, Zhou J (2012) Overexpression of CXCL5 mediates neutrophil infiltration and indicates poor prognosis for hepatocellular carcinoma. Hepatology. doi:10.​1002/​hep.​25907 [Epub ahead of print]
43.
go back to reference Okabe H, Beppu T, Ueda M, Hayashi H, Ishiko T, Masuda T, Otao R, Horlad H, Mima K, Miyake K, Iwatsuki M, Baba Y, Takamori H, Jono H, Shinriki S, Ando Y, Baba H (2012) Identification of CXCL5/ENA-78 as a factor involved in the interaction between cholangiocarcinoma cells and cancer-associated fibroblasts. Int J Cancer. doi:10.1002/ijc.27496 [Epub ahead of print] Okabe H, Beppu T, Ueda M, Hayashi H, Ishiko T, Masuda T, Otao R, Horlad H, Mima K, Miyake K, Iwatsuki M, Baba Y, Takamori H, Jono H, Shinriki S, Ando Y, Baba H (2012) Identification of CXCL5/ENA-78 as a factor involved in the interaction between cholangiocarcinoma cells and cancer-associated fibroblasts. Int J Cancer. doi:10.​1002/​ijc.​27496 [Epub ahead of print]
44.
go back to reference Gao Q, Zhao YJ, Wang XY, Qiu SJ, Shi YH, Sun J, Yi Y, Shi JY, Shi GM, Ding ZB, Xiao YS, Zhao ZH, Zhou J, He XH, Fan J (2012) CXCR6 upregulation contributes to a proinflammatory tumor microenvironment that drives metastasis and poor patient outcomes in hepatocellular carcinoma. Cancer Res 72(14):3546–3556PubMedCrossRef Gao Q, Zhao YJ, Wang XY, Qiu SJ, Shi YH, Sun J, Yi Y, Shi JY, Shi GM, Ding ZB, Xiao YS, Zhao ZH, Zhou J, He XH, Fan J (2012) CXCR6 upregulation contributes to a proinflammatory tumor microenvironment that drives metastasis and poor patient outcomes in hepatocellular carcinoma. Cancer Res 72(14):3546–3556PubMedCrossRef
45.
go back to reference Trellakis S, Bruderek K, Dumitru CA, Gholaman H, Gu X, Bankfalvi A, Scherag A, Hutte J, Dominas N, Lehnerdt GF, Hoffmann TK, Lang S, Brandau S (2011) Polymorphonuclear granulocytes in human head and neck cancer: enhanced inflammatory activity, modulation by cancer cells and expansion in advanced disease. Int J Cancer 129:2183–2193PubMedCrossRef Trellakis S, Bruderek K, Dumitru CA, Gholaman H, Gu X, Bankfalvi A, Scherag A, Hutte J, Dominas N, Lehnerdt GF, Hoffmann TK, Lang S, Brandau S (2011) Polymorphonuclear granulocytes in human head and neck cancer: enhanced inflammatory activity, modulation by cancer cells and expansion in advanced disease. Int J Cancer 129:2183–2193PubMedCrossRef
46.
go back to reference Bernhagen J, Krohn R, Lue H, Gregory JL, Zernecke A, Koenen RR, Dewor M, Georgiev I, Schober A, Leng L, Kooistra T, Fingerle-Rowson G, Ghezzi P, Kleemann R, McColl SR, Bucala R, Hickey MJ, Weber C (2007) MIF is a noncognate ligand of CXC chemokine receptors in inflammatory and atherogenic cell recruitment. Nat Med 13:587–596PubMedCrossRef Bernhagen J, Krohn R, Lue H, Gregory JL, Zernecke A, Koenen RR, Dewor M, Georgiev I, Schober A, Leng L, Kooistra T, Fingerle-Rowson G, Ghezzi P, Kleemann R, McColl SR, Bucala R, Hickey MJ, Weber C (2007) MIF is a noncognate ligand of CXC chemokine receptors in inflammatory and atherogenic cell recruitment. Nat Med 13:587–596PubMedCrossRef
47.
go back to reference Dumitru CA, Gholaman H, Trellakis S, Bruderek K, Dominas N, Gu X, Bankfalvi A, Whiteside TL, Lang S, Brandau S (2011) Tumor-derived macrophage migration inhibitory factor modulates the biology of head and neck cancer cells via neutrophil activation. Int J Cancer 129:859–869PubMedCrossRef Dumitru CA, Gholaman H, Trellakis S, Bruderek K, Dominas N, Gu X, Bankfalvi A, Whiteside TL, Lang S, Brandau S (2011) Tumor-derived macrophage migration inhibitory factor modulates the biology of head and neck cancer cells via neutrophil activation. Int J Cancer 129:859–869PubMedCrossRef
48.
go back to reference Florey O, Haskard DO (2009) Sphingosine 1-phosphate enhances Fc gamma receptor-mediated neutrophil activation and recruitment under flow conditions. J Immunol 183:2330–2336PubMedCrossRef Florey O, Haskard DO (2009) Sphingosine 1-phosphate enhances Fc gamma receptor-mediated neutrophil activation and recruitment under flow conditions. J Immunol 183:2330–2336PubMedCrossRef
49.
go back to reference Gault CR, Obeid LM (2011) Still benched on its way to the bedside: sphingosine kinase 1 as an emerging target in cancer chemotherapy. Crit Rev Biochem Mol Biol 46:342–351PubMedCrossRef Gault CR, Obeid LM (2011) Still benched on its way to the bedside: sphingosine kinase 1 as an emerging target in cancer chemotherapy. Crit Rev Biochem Mol Biol 46:342–351PubMedCrossRef
50.
go back to reference Jamieson NB, Carter CR, McKay CJ, Oien KA (2011) Tissue biomarkers for prognosis in pancreatic ductal adenocarcinoma: a systematic review and meta-analysis. Clin Cancer Res 17:3316–3331PubMedCrossRef Jamieson NB, Carter CR, McKay CJ, Oien KA (2011) Tissue biomarkers for prognosis in pancreatic ductal adenocarcinoma: a systematic review and meta-analysis. Clin Cancer Res 17:3316–3331PubMedCrossRef
51.
go back to reference Tang D, Kang R, Zeh HJ III, Lotze MT (2010) High-mobility group box 1 and cancer. Biochim Biophys Acta 1799:131–140PubMedCrossRef Tang D, Kang R, Zeh HJ III, Lotze MT (2010) High-mobility group box 1 and cancer. Biochim Biophys Acta 1799:131–140PubMedCrossRef
52.
go back to reference Orlova VV, Choi EY, Xie C, Chavakis E, Bierhaus A, Ihanus E, Ballantyne CM, Gahmberg CG, Bianchi ME, Nawroth PP, Chavakis T (2007) A novel pathway of HMGB1-mediated inflammatory cell recruitment that requires Mac-1-integrin. EMBO J 26:1129–1139PubMedCrossRef Orlova VV, Choi EY, Xie C, Chavakis E, Bierhaus A, Ihanus E, Ballantyne CM, Gahmberg CG, Bianchi ME, Nawroth PP, Chavakis T (2007) A novel pathway of HMGB1-mediated inflammatory cell recruitment that requires Mac-1-integrin. EMBO J 26:1129–1139PubMedCrossRef
53.
go back to reference Ryckman C, Vandal K, Rouleau P, Talbot M, Tessier PA (2003) Proinflammatory activities of S100: proteins S100A8, S100A9, and S100A8/A9 induce neutrophil chemotaxis and adhesion. J Immunol 170:3233–3242PubMed Ryckman C, Vandal K, Rouleau P, Talbot M, Tessier PA (2003) Proinflammatory activities of S100: proteins S100A8, S100A9, and S100A8/A9 induce neutrophil chemotaxis and adhesion. J Immunol 170:3233–3242PubMed
54.
go back to reference Zhao JJ, Pan K, Wang W, Chen JG, Wu YH, Lv L, Li JJ, Chen YB, Wang DD, Pan QZ, Li XD, Xia JC (2012) The prognostic value of tumor-infiltrating neutrophils in gastric adenocarcinoma after resection. PLoS One 7:e33655PubMedCrossRef Zhao JJ, Pan K, Wang W, Chen JG, Wu YH, Lv L, Li JJ, Chen YB, Wang DD, Pan QZ, Li XD, Xia JC (2012) The prognostic value of tumor-infiltrating neutrophils in gastric adenocarcinoma after resection. PLoS One 7:e33655PubMedCrossRef
55.
go back to reference Rao HL, Chen JW, Li M, Xiao YB, Fu J, Zeng YX, Cai MY, Xie D (2012) Increased intratumoral neutrophil in colorectal carcinomas correlates closely with malignant phenotype and predicts patients’ adverse prognosis. PLoS One 7:e30806PubMedCrossRef Rao HL, Chen JW, Li M, Xiao YB, Fu J, Zeng YX, Cai MY, Xie D (2012) Increased intratumoral neutrophil in colorectal carcinomas correlates closely with malignant phenotype and predicts patients’ adverse prognosis. PLoS One 7:e30806PubMedCrossRef
56.
go back to reference Nozawa H, Chiu C, Hanahan D (2006) Infiltrating neutrophils mediate the initial angiogenic switch in a mouse model of multistage carcinogenesis. Proc Natl Acad Sci U S A 103:12493–12498PubMedCrossRef Nozawa H, Chiu C, Hanahan D (2006) Infiltrating neutrophils mediate the initial angiogenic switch in a mouse model of multistage carcinogenesis. Proc Natl Acad Sci U S A 103:12493–12498PubMedCrossRef
57.
go back to reference Jablonska J, Leschner S, Westphal K, Lienenklaus S, Weiss S (2010) Neutrophils responsive to endogenous IFN-beta regulate tumor angiogenesis and growth in a mouse tumor model. J Clin Invest 120:1151–1164PubMedCrossRef Jablonska J, Leschner S, Westphal K, Lienenklaus S, Weiss S (2010) Neutrophils responsive to endogenous IFN-beta regulate tumor angiogenesis and growth in a mouse tumor model. J Clin Invest 120:1151–1164PubMedCrossRef
58.
go back to reference Bekes EM, Schweighofer B, Kupriyanova TA, Zajac E, Ardi VC, Quigley JP, Deryugina EI (2011) Tumor-recruited neutrophils and neutrophil TIMP-free MMP-9 regulate coordinately the levels of tumor angiogenesis and efficiency of malignant cell intravasation. Am J Pathol 179:1455–1470PubMedCrossRef Bekes EM, Schweighofer B, Kupriyanova TA, Zajac E, Ardi VC, Quigley JP, Deryugina EI (2011) Tumor-recruited neutrophils and neutrophil TIMP-free MMP-9 regulate coordinately the levels of tumor angiogenesis and efficiency of malignant cell intravasation. Am J Pathol 179:1455–1470PubMedCrossRef
59.
go back to reference Dumitru CA, Fechner MK, Hoffmann TK, Lang S, Brandau S (2012) A novel p38-MAPK signaling axis modulates neutrophil biology in head and neck cancer. J Leukoc Biol 91:591–598PubMedCrossRef Dumitru CA, Fechner MK, Hoffmann TK, Lang S, Brandau S (2012) A novel p38-MAPK signaling axis modulates neutrophil biology in head and neck cancer. J Leukoc Biol 91:591–598PubMedCrossRef
60.
go back to reference Kuang DM, Zhao Q, Wu Y, Peng C, Wang J, Xu Z, Yin XY, Zheng L (2011) Peritumoral neutrophils link inflammatory response to disease progression by fostering angiogenesis in hepatocellular carcinoma. J Hepatol 54:948–955PubMedCrossRef Kuang DM, Zhao Q, Wu Y, Peng C, Wang J, Xu Z, Yin XY, Zheng L (2011) Peritumoral neutrophils link inflammatory response to disease progression by fostering angiogenesis in hepatocellular carcinoma. J Hepatol 54:948–955PubMedCrossRef
61.
go back to reference Wu Y, Zhao Q, Peng C, Sun L, Li XF, Kuang DM (2011) Neutrophils promote motility of cancer cells via a hyaluronan-mediated TLR4/PI3K activation loop. J Pathol 225:438–447PubMedCrossRef Wu Y, Zhao Q, Peng C, Sun L, Li XF, Kuang DM (2011) Neutrophils promote motility of cancer cells via a hyaluronan-mediated TLR4/PI3K activation loop. J Pathol 225:438–447PubMedCrossRef
62.
go back to reference Strell C, Lang K, Niggemann B, Zaenker KS, Entschladen F (2010) Neutrophil granulocytes promote the migratory activity of MDA-MB-468 human breast carcinoma cells via ICAM-1. Exp Cell Res 316:138–148PubMedCrossRef Strell C, Lang K, Niggemann B, Zaenker KS, Entschladen F (2010) Neutrophil granulocytes promote the migratory activity of MDA-MB-468 human breast carcinoma cells via ICAM-1. Exp Cell Res 316:138–148PubMedCrossRef
63.
go back to reference Shamamian P, Schwartz JD, Pocock BJ, Monea S, Whiting D, Marcus SG, Mignatti P (2001) Activation of progelatinase A (MMP-2) by neutrophil elastase, cathepsin G, and proteinase-3: a role for inflammatory cells in tumor invasion and angiogenesis. J Cell Physiol 189:197–206PubMedCrossRef Shamamian P, Schwartz JD, Pocock BJ, Monea S, Whiting D, Marcus SG, Mignatti P (2001) Activation of progelatinase A (MMP-2) by neutrophil elastase, cathepsin G, and proteinase-3: a role for inflammatory cells in tumor invasion and angiogenesis. J Cell Physiol 189:197–206PubMedCrossRef
64.
go back to reference Queen MM, Ryan RE, Holzer RG, Keller-Peck CR, Jorcyk CL (2005) Breast cancer cells stimulate neutrophils to produce oncostatin M: potential implications for tumor progression. Cancer Res 65:8896–8904PubMedCrossRef Queen MM, Ryan RE, Holzer RG, Keller-Peck CR, Jorcyk CL (2005) Breast cancer cells stimulate neutrophils to produce oncostatin M: potential implications for tumor progression. Cancer Res 65:8896–8904PubMedCrossRef
65.
go back to reference Imai Y, Kubota Y, Yamamoto S, Tsuji K, Shimatani M, Shibatani N, Takamido S, Matsushita M, Okazaki K (2005) Neutrophils enhance invasion activity of human cholangiocellular carcinoma and hepatocellular carcinoma cells: an in vitro study. J Gastroenterol Hepatol 20:287–293PubMedCrossRef Imai Y, Kubota Y, Yamamoto S, Tsuji K, Shimatani M, Shibatani N, Takamido S, Matsushita M, Okazaki K (2005) Neutrophils enhance invasion activity of human cholangiocellular carcinoma and hepatocellular carcinoma cells: an in vitro study. J Gastroenterol Hepatol 20:287–293PubMedCrossRef
66.
go back to reference Tazawa H, Okada F, Kobayashi T, Tada M, Mori Y, Une Y, Sendo F, Kobayashi M, Hosokawa M (2003) Infiltration of neutrophils is required for acquisition of metastatic phenotype of benign murine fibrosarcoma cells: implication of inflammation-associated carcinogenesis and tumor progression. Am J Pathol 163:2221–2232PubMedCrossRef Tazawa H, Okada F, Kobayashi T, Tada M, Mori Y, Une Y, Sendo F, Kobayashi M, Hosokawa M (2003) Infiltration of neutrophils is required for acquisition of metastatic phenotype of benign murine fibrosarcoma cells: implication of inflammation-associated carcinogenesis and tumor progression. Am J Pathol 163:2221–2232PubMedCrossRef
67.
68.
go back to reference Psaila B, Lyden D (2009) The metastatic niche: adapting the foreign soil. Nat Rev Cancer 9:285–293PubMedCrossRef Psaila B, Lyden D (2009) The metastatic niche: adapting the foreign soil. Nat Rev Cancer 9:285–293PubMedCrossRef
69.
go back to reference Yan HH, Pickup M, Pang Y, Gorska AE, Li Z, Chytil A, Geng Y, Gray JW, Moses HL, Yang L (2010) Gr-1+CD11b+ myeloid cells tip the balance of immune protection to tumor promotion in the premetastatic lung. Cancer Res 70:6139–6149PubMedCrossRef Yan HH, Pickup M, Pang Y, Gorska AE, Li Z, Chytil A, Geng Y, Gray JW, Moses HL, Yang L (2010) Gr-1+CD11b+ myeloid cells tip the balance of immune protection to tumor promotion in the premetastatic lung. Cancer Res 70:6139–6149PubMedCrossRef
70.
go back to reference Kowanetz M, Wu X, Lee J, Tan M, Hagenbeek T, Qu X, Yu L, Ross J, Korsisaari N, Cao T, Bou-Reslan H, Kallop D, Weimer R, Ludlam MJ, Kaminker JS, Modrusan Z, van Bruggen N, Peale FV, Carano R, Meng YG, Ferrara N (2010) Granulocyte-colony stimulating factor promotes lung metastasis through mobilization of Ly6G+Ly6C+ granulocytes. Proc Natl Acad Sci U S A 107:21248–21255PubMedCrossRef Kowanetz M, Wu X, Lee J, Tan M, Hagenbeek T, Qu X, Yu L, Ross J, Korsisaari N, Cao T, Bou-Reslan H, Kallop D, Weimer R, Ludlam MJ, Kaminker JS, Modrusan Z, van Bruggen N, Peale FV, Carano R, Meng YG, Ferrara N (2010) Granulocyte-colony stimulating factor promotes lung metastasis through mobilization of Ly6G+Ly6C+ granulocytes. Proc Natl Acad Sci U S A 107:21248–21255PubMedCrossRef
71.
go back to reference Sceneay J, Chow MT, Chen A, Halse HM, Wong CS, Andrews DM, Sloan EK, Parker BS, Bowtell DD, Smyth MJ, Moller A (2012) Primary tumor hypoxia recruits CD11b+/Ly6Cmed/Ly6G+ immune suppressor cells and compromises NK cell cytotoxicity in the premetastatic niche. Cancer Res 72:3906–3911 Sceneay J, Chow MT, Chen A, Halse HM, Wong CS, Andrews DM, Sloan EK, Parker BS, Bowtell DD, Smyth MJ, Moller A (2012) Primary tumor hypoxia recruits CD11b+/Ly6Cmed/Ly6G+ immune suppressor cells and compromises NK cell cytotoxicity in the premetastatic niche. Cancer Res 72:3906–3911
72.
go back to reference Tazzyman S, Barry ST, Ashton S, Wood P, Blakey D, Lewis CE, Murdoch C (2011) Inhibition of neutrophil infiltration into A549 lung tumors in vitro and in vivo using a CXCR2-specific antagonist is associated with reduced tumor growth. Int J Cancer 129:847–858PubMedCrossRef Tazzyman S, Barry ST, Ashton S, Wood P, Blakey D, Lewis CE, Murdoch C (2011) Inhibition of neutrophil infiltration into A549 lung tumors in vitro and in vivo using a CXCR2-specific antagonist is associated with reduced tumor growth. Int J Cancer 129:847–858PubMedCrossRef
73.
go back to reference Wada Y, Yoshida K, Tsutani Y, Shigematsu H, Oeda M, Sanada Y, Suzuki T, Mizuiri H, Hamai Y, Tanabe K, Ukon K, Hihara J (2007) Neutrophil elastase induces cell proliferation and migration by the release of TGF-alpha, PDGF and VEGF in esophageal cell lines. Oncol Rep 17:161–167PubMed Wada Y, Yoshida K, Tsutani Y, Shigematsu H, Oeda M, Sanada Y, Suzuki T, Mizuiri H, Hamai Y, Tanabe K, Ukon K, Hihara J (2007) Neutrophil elastase induces cell proliferation and migration by the release of TGF-alpha, PDGF and VEGF in esophageal cell lines. Oncol Rep 17:161–167PubMed
74.
go back to reference Giese A, Bjerkvig R, Berens ME, Westphal M (2003) Cost of migration: invasion of malignant gliomas and implications for treatment. J Clin Oncol 21:1624–1636PubMedCrossRef Giese A, Bjerkvig R, Berens ME, Westphal M (2003) Cost of migration: invasion of malignant gliomas and implications for treatment. J Clin Oncol 21:1624–1636PubMedCrossRef
75.
go back to reference Jung A, Schrauder M, Oswald U, Knoll C, Sellberg P, Palmqvist R, Niedobitek G, Brabletz T, Kirchner T (2001) The invasion front of human colorectal adenocarcinomas shows co-localization of nuclear beta-catenin, cyclin D1, and p16INK4A and is a region of low proliferation. Am J Pathol 159:1613–1617PubMedCrossRef Jung A, Schrauder M, Oswald U, Knoll C, Sellberg P, Palmqvist R, Niedobitek G, Brabletz T, Kirchner T (2001) The invasion front of human colorectal adenocarcinomas shows co-localization of nuclear beta-catenin, cyclin D1, and p16INK4A and is a region of low proliferation. Am J Pathol 159:1613–1617PubMedCrossRef
76.
go back to reference Fridlender ZG, Sun J, Kim S, Kapoor V, Cheng G, Ling L, Worthen GS, Albelda SM (2009) Polarization of tumor-associated neutrophil phenotype by TGF-beta: “N1” versus “N2” TAN. Cancer Cell 16:183–194PubMedCrossRef Fridlender ZG, Sun J, Kim S, Kapoor V, Cheng G, Ling L, Worthen GS, Albelda SM (2009) Polarization of tumor-associated neutrophil phenotype by TGF-beta: “N1” versus “N2” TAN. Cancer Cell 16:183–194PubMedCrossRef
77.
go back to reference Rotondo R, Barisione G, Mastracci L, Grossi F, Orengo AM, Costa R, Truini M, Fabbi M, Ferrini S, Barbieri O (2009) IL-8 induces exocytosis of arginase 1 by neutrophil polymorphonuclears in nonsmall cell lung cancer. Int J Cancer 125:887–893PubMedCrossRef Rotondo R, Barisione G, Mastracci L, Grossi F, Orengo AM, Costa R, Truini M, Fabbi M, Ferrini S, Barbieri O (2009) IL-8 induces exocytosis of arginase 1 by neutrophil polymorphonuclears in nonsmall cell lung cancer. Int J Cancer 125:887–893PubMedCrossRef
78.
go back to reference Mantovani A, Cassatella MA, Costantini C, Jaillon S (2011) Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol 11:519–531PubMedCrossRef Mantovani A, Cassatella MA, Costantini C, Jaillon S (2011) Neutrophils in the activation and regulation of innate and adaptive immunity. Nat Rev Immunol 11:519–531PubMedCrossRef
79.
go back to reference Pickaver AH, Ratcliffe NA, Williams AE, Smith H (1972) Cytotoxic effects of peritoneal neutrophils on a syngeneic rat tumour. Nat New Biol 235:186–187PubMed Pickaver AH, Ratcliffe NA, Williams AE, Smith H (1972) Cytotoxic effects of peritoneal neutrophils on a syngeneic rat tumour. Nat New Biol 235:186–187PubMed
80.
go back to reference Souto JC, Vila L, Bru A (2011) Polymorphonuclear neutrophils and cancer: intense and sustained neutrophilia as a treatment against solid tumors. Med Res Rev 31:311–363PubMedCrossRef Souto JC, Vila L, Bru A (2011) Polymorphonuclear neutrophils and cancer: intense and sustained neutrophilia as a treatment against solid tumors. Med Res Rev 31:311–363PubMedCrossRef
81.
go back to reference van Egmond M (2008) Neutrophils in antibody-based immunotherapy of cancer. Expert Opin Biol Ther 8:83–94PubMedCrossRef van Egmond M (2008) Neutrophils in antibody-based immunotherapy of cancer. Expert Opin Biol Ther 8:83–94PubMedCrossRef
82.
go back to reference Ottonello L, Epstein AL, Mancini M, Tortolina G, Dapino P, Dallegri F (2001) Chimaeric Lym-1 monoclonal antibody-mediated cytolysis by neutrophils from G-CSF-treated patients: stimulation by GM-CSF and role of Fc gamma-receptors. Br J Cancer 85:463–469PubMedCrossRef Ottonello L, Epstein AL, Mancini M, Tortolina G, Dapino P, Dallegri F (2001) Chimaeric Lym-1 monoclonal antibody-mediated cytolysis by neutrophils from G-CSF-treated patients: stimulation by GM-CSF and role of Fc gamma-receptors. Br J Cancer 85:463–469PubMedCrossRef
83.
go back to reference Cassatella MA, Flynn RM, Amezaga MA, Bazzoni F, Vicentini F, Trinchieri G (1990) Interferon gamma induces in human neutrophils and macrophages expression of the mRNA for the high affinity receptor for monomeric IgG (Fc gamma R-I or CD64). Biochem Biophys Res Commun 170:582–588PubMedCrossRef Cassatella MA, Flynn RM, Amezaga MA, Bazzoni F, Vicentini F, Trinchieri G (1990) Interferon gamma induces in human neutrophils and macrophages expression of the mRNA for the high affinity receptor for monomeric IgG (Fc gamma R-I or CD64). Biochem Biophys Res Commun 170:582–588PubMedCrossRef
84.
go back to reference Valerius T, Repp R, de Wit TP, Berthold S, Platzer E, Kalden JR, Gramatzki M, van de Winkel JG (1993) Involvement of the high-affinity receptor for IgG (Fc gamma RI; CD64) in enhanced tumor cell cytotoxicity of neutrophils during granulocyte colony-stimulating factor therapy. Blood 82:931–939PubMed Valerius T, Repp R, de Wit TP, Berthold S, Platzer E, Kalden JR, Gramatzki M, van de Winkel JG (1993) Involvement of the high-affinity receptor for IgG (Fc gamma RI; CD64) in enhanced tumor cell cytotoxicity of neutrophils during granulocyte colony-stimulating factor therapy. Blood 82:931–939PubMed
85.
go back to reference Su YB, Vickers AJ, Zelefsky MJ, Kraus DH, Shaha AR, Shah JP, Serio AM, Harrison LB, Bosl GJ, Pfister DG (2006) Double-blind, placebo-controlled, randomized trial of granulocyte-colony stimulating factor during postoperative radiotherapy for squamous head and neck cancer. Cancer J 12:182–188PubMedCrossRef Su YB, Vickers AJ, Zelefsky MJ, Kraus DH, Shaha AR, Shah JP, Serio AM, Harrison LB, Bosl GJ, Pfister DG (2006) Double-blind, placebo-controlled, randomized trial of granulocyte-colony stimulating factor during postoperative radiotherapy for squamous head and neck cancer. Cancer J 12:182–188PubMedCrossRef
86.
go back to reference Otten MA, Rudolph E, Dechant M, Tuk CW, Reijmers RM, Beelen RH, van de Winkel JG, van Egmond M (2005) Immature neutrophils mediate tumor cell killing via IgA but not IgG Fc receptors. J Immunol 174:5472–5480PubMed Otten MA, Rudolph E, Dechant M, Tuk CW, Reijmers RM, Beelen RH, van de Winkel JG, van Egmond M (2005) Immature neutrophils mediate tumor cell killing via IgA but not IgG Fc receptors. J Immunol 174:5472–5480PubMed
87.
go back to reference Huls G, Heijnen IA, Cuomo E, van der Linden J, Boel E, van de Winkel JG, Logtenberg T (1999) Antitumor immune effector mechanisms recruited by phage display-derived fully human IgG1 and IgA1 monoclonal antibodies. Cancer Res 59:5778–5784PubMed Huls G, Heijnen IA, Cuomo E, van der Linden J, Boel E, van de Winkel JG, Logtenberg T (1999) Antitumor immune effector mechanisms recruited by phage display-derived fully human IgG1 and IgA1 monoclonal antibodies. Cancer Res 59:5778–5784PubMed
88.
go back to reference Theilgaard-Monch K, Jacobsen LC, Borup R, Rasmussen T, Bjerregaard MD, Nielsen FC, Cowland JB, Borregaard N (2005) The transcriptional program of terminal granulocytic differentiation. Blood 105:1785–1796PubMedCrossRef Theilgaard-Monch K, Jacobsen LC, Borup R, Rasmussen T, Bjerregaard MD, Nielsen FC, Cowland JB, Borregaard N (2005) The transcriptional program of terminal granulocytic differentiation. Blood 105:1785–1796PubMedCrossRef
89.
go back to reference Dallegri F, Patrone F, Frumento G, Sacchetti C (1984) Antibody-dependent killing of tumor cells by polymorphonuclear leukocytes. Involvement of oxidative and nonoxidative mechanisms. J Natl Cancer Inst 73:331–339PubMed Dallegri F, Patrone F, Frumento G, Sacchetti C (1984) Antibody-dependent killing of tumor cells by polymorphonuclear leukocytes. Involvement of oxidative and nonoxidative mechanisms. J Natl Cancer Inst 73:331–339PubMed
90.
go back to reference Dallegri F, Ottonello L, Ballestrero A, Dapino P, Ferrando F, Patrone F, Sacchetti C (1991) Tumor cell lysis by activated human neutrophils: analysis of neutrophil-delivered oxidative attack and role of leukocyte function-associated antigen 1. Inflammation 15:15–30PubMedCrossRef Dallegri F, Ottonello L, Ballestrero A, Dapino P, Ferrando F, Patrone F, Sacchetti C (1991) Tumor cell lysis by activated human neutrophils: analysis of neutrophil-delivered oxidative attack and role of leukocyte function-associated antigen 1. Inflammation 15:15–30PubMedCrossRef
91.
go back to reference Clark RA, Klebanoff SJ (1975) Neutrophil-mediated tumor cell cytotoxicity: role of the peroxidase system. J Exp Med 141:1442–1447PubMedCrossRef Clark RA, Klebanoff SJ (1975) Neutrophil-mediated tumor cell cytotoxicity: role of the peroxidase system. J Exp Med 141:1442–1447PubMedCrossRef
92.
go back to reference Kushner BH, Cheung NK (1991) Clinically effective monoclonal antibody 3F8 mediates nonoxidative lysis of human neuroectodermal tumor cells by polymorphonuclear leukocytes. Cancer Res 51:4865–4870PubMed Kushner BH, Cheung NK (1991) Clinically effective monoclonal antibody 3F8 mediates nonoxidative lysis of human neuroectodermal tumor cells by polymorphonuclear leukocytes. Cancer Res 51:4865–4870PubMed
93.
go back to reference Grossman WJ, Ley TJ (2004) Granzymes A and B are not expressed in human neutrophils. Blood 104:906–907PubMedCrossRef Grossman WJ, Ley TJ (2004) Granzymes A and B are not expressed in human neutrophils. Blood 104:906–907PubMedCrossRef
94.
go back to reference Metkar SS, Froelich CJ (2004) Human neutrophils lack granzyme A, granzyme B, and perforin. Blood 104:905–906PubMedCrossRef Metkar SS, Froelich CJ (2004) Human neutrophils lack granzyme A, granzyme B, and perforin. Blood 104:905–906PubMedCrossRef
95.
go back to reference Wagner C, Iking-Konert C, Denefleh B, Stegmaier S, Hug F, Hansch GM (2004) Granzyme B and perforin: constitutive expression in human polymorphonuclear neutrophils. Blood 103:1099–1104PubMedCrossRef Wagner C, Iking-Konert C, Denefleh B, Stegmaier S, Hug F, Hansch GM (2004) Granzyme B and perforin: constitutive expression in human polymorphonuclear neutrophils. Blood 103:1099–1104PubMedCrossRef
96.
go back to reference Hubert P, Heitzmann A, Viel S, Nicolas A, Sastre-Garau X, Oppezzo P, Pritsch O, Osinaga E, Amigorena S (2011) Antibody-dependent cell cytotoxicity synapses form in mice during tumor-specific antibody immunotherapy. Cancer Res 71:5134–5143PubMedCrossRef Hubert P, Heitzmann A, Viel S, Nicolas A, Sastre-Garau X, Oppezzo P, Pritsch O, Osinaga E, Amigorena S (2011) Antibody-dependent cell cytotoxicity synapses form in mice during tumor-specific antibody immunotherapy. Cancer Res 71:5134–5143PubMedCrossRef
97.
go back to reference Bakema JE, Ganzevles SH, Fluitsma DM, Schilham MW, Beelen RH, Valerius T, Lohse S, Glennie MJ, Medema JP, van Egmond M (2011) Targeting FcαRI on polymorphonuclear cells induces tumor cell killing through autophagy. J Immunol 187:726–732PubMedCrossRef Bakema JE, Ganzevles SH, Fluitsma DM, Schilham MW, Beelen RH, Valerius T, Lohse S, Glennie MJ, Medema JP, van Egmond M (2011) Targeting FcαRI on polymorphonuclear cells induces tumor cell killing through autophagy. J Immunol 187:726–732PubMedCrossRef
98.
go back to reference Otten MA, Bakema JE, Tuk CW, Glennie MJ, Tutt AL, Beelen RH, van de Winkel JG, van Egmond M (2012) Enhanced FcαRI-mediated neutrophil migration towards tumour colonies in the presence of endothelial cells. Eur J Immunol 42(7):1815–1821PubMedCrossRef Otten MA, Bakema JE, Tuk CW, Glennie MJ, Tutt AL, Beelen RH, van de Winkel JG, van Egmond M (2012) Enhanced FcαRI-mediated neutrophil migration towards tumour colonies in the presence of endothelial cells. Eur J Immunol 42(7):1815–1821PubMedCrossRef
99.
go back to reference van Spriel AB, Leusen JH, van Egmond M, Dijkman HB, Assmann KJ, Mayadas TN, van de Winkel JG (2001) Mac-1 (CD11b/CD18) is essential for Fc receptor-mediated neutrophil cytotoxicity and immunologic synapse formation. Blood 97:2478–2486PubMedCrossRef van Spriel AB, Leusen JH, van Egmond M, Dijkman HB, Assmann KJ, Mayadas TN, van de Winkel JG (2001) Mac-1 (CD11b/CD18) is essential for Fc receptor-mediated neutrophil cytotoxicity and immunologic synapse formation. Blood 97:2478–2486PubMedCrossRef
100.
go back to reference Galluzzi L, Vacchelli E, Eggermont A, Fridman WH, Galon J, Sautes-Fridman C, Tartour E, Zitvogel L, Kroemer G (2012) Trial watch: experimental toll-like receptor agonists for cancer therapy. Oncoimmunology 1(5):699–716PubMedCrossRef Galluzzi L, Vacchelli E, Eggermont A, Fridman WH, Galon J, Sautes-Fridman C, Tartour E, Zitvogel L, Kroemer G (2012) Trial watch: experimental toll-like receptor agonists for cancer therapy. Oncoimmunology 1(5):699–716PubMedCrossRef
101.
go back to reference Tadie JM, Bae HB, Banerjee S, Zmijewski JW, Abraham E (2012) Differential activation of RAGE by HMGB1 modulates neutrophil-associated NADPH oxidase activity and bacterial killing. Am J Physiol Cell Physiol 302:C249–C256PubMedCrossRef Tadie JM, Bae HB, Banerjee S, Zmijewski JW, Abraham E (2012) Differential activation of RAGE by HMGB1 modulates neutrophil-associated NADPH oxidase activity and bacterial killing. Am J Physiol Cell Physiol 302:C249–C256PubMedCrossRef
102.
go back to reference Kawai T, Akira S (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 11:373–384PubMedCrossRef Kawai T, Akira S (2010) The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat Immunol 11:373–384PubMedCrossRef
103.
go back to reference Kersse K, Bertrand MJ, Lamkanfi M, Vandenabeele P (2011) NOD-like receptors and the innate immune system: coping with danger, damage and death. Cytokine Growth Factor Rev 22:257–276PubMedCrossRef Kersse K, Bertrand MJ, Lamkanfi M, Vandenabeele P (2011) NOD-like receptors and the innate immune system: coping with danger, damage and death. Cytokine Growth Factor Rev 22:257–276PubMedCrossRef
104.
go back to reference Kandasamy M, Bay BH, Lee YK, Mahendran R (2011) Lactobacilli secreting a tumor antigen and IL15 activates neutrophils and dendritic cells and generates cytotoxic T lymphocytes against cancer cells. Cell Immunol 271:89–96PubMedCrossRef Kandasamy M, Bay BH, Lee YK, Mahendran R (2011) Lactobacilli secreting a tumor antigen and IL15 activates neutrophils and dendritic cells and generates cytotoxic T lymphocytes against cancer cells. Cell Immunol 271:89–96PubMedCrossRef
105.
go back to reference Suttmann H, Riemensberger J, Bentien G, Schmaltz D, Stockle M, Jocham D, Bohle A, Brandau S (2006) Neutrophil granulocytes are required for effective Bacillus Calmette–Guerin immunotherapy of bladder cancer and orchestrate local immune responses. Cancer Res 66:8250–8257PubMedCrossRef Suttmann H, Riemensberger J, Bentien G, Schmaltz D, Stockle M, Jocham D, Bohle A, Brandau S (2006) Neutrophil granulocytes are required for effective Bacillus Calmette–Guerin immunotherapy of bladder cancer and orchestrate local immune responses. Cancer Res 66:8250–8257PubMedCrossRef
106.
go back to reference Brandau S, Suttmann H (2007) Thirty years of BCG immunotherapy for non-muscle invasive bladder cancer: a success story with room for improvement. Biomed Pharmacother 61:299–305PubMedCrossRef Brandau S, Suttmann H (2007) Thirty years of BCG immunotherapy for non-muscle invasive bladder cancer: a success story with room for improvement. Biomed Pharmacother 61:299–305PubMedCrossRef
107.
go back to reference Cassatella MA (1999) Neutrophil-derived proteins: selling cytokines by the pound. Adv Immunol 73:369–509PubMedCrossRef Cassatella MA (1999) Neutrophil-derived proteins: selling cytokines by the pound. Adv Immunol 73:369–509PubMedCrossRef
108.
go back to reference Rosevear HM, Lightfoot AJ, O’Donnell MA, Griffith TS (2009) The role of neutrophils and TNF-related apoptosis-inducing ligand (TRAIL) in bacillus Calmette–Guerin (BCG) immunotherapy for urothelial carcinoma of the bladder. Cancer Metastasis Rev 28:345–353PubMedCrossRef Rosevear HM, Lightfoot AJ, O’Donnell MA, Griffith TS (2009) The role of neutrophils and TNF-related apoptosis-inducing ligand (TRAIL) in bacillus Calmette–Guerin (BCG) immunotherapy for urothelial carcinoma of the bladder. Cancer Metastasis Rev 28:345–353PubMedCrossRef
109.
go back to reference Mittendorf EA, Alatrash G, Qiao N, Wu Y, Sukhumalchandra P, St John LS, Philips AV, Xiao H, Zhang M, Ruisaard K, Clise-Dwyer K, Lu S, Molldrem JJ (2012) Breast cancer cell uptake of the inflammatory mediator neutrophil elastase triggers an anticancer adaptive immune response. Cancer Res 72:3153–3162PubMedCrossRef Mittendorf EA, Alatrash G, Qiao N, Wu Y, Sukhumalchandra P, St John LS, Philips AV, Xiao H, Zhang M, Ruisaard K, Clise-Dwyer K, Lu S, Molldrem JJ (2012) Breast cancer cell uptake of the inflammatory mediator neutrophil elastase triggers an anticancer adaptive immune response. Cancer Res 72:3153–3162PubMedCrossRef
110.
go back to reference Li B, Allendorf DJ, Hansen R, Marroquin J, Cramer DE, Harris CL, Yan J (2007) Combined yeast {beta}-glucan and antitumor monoclonal antibody therapy requires C5a-mediated neutrophil chemotaxis via regulation of decay-accelerating factor CD55. Cancer Res 67:7421–7430PubMedCrossRef Li B, Allendorf DJ, Hansen R, Marroquin J, Cramer DE, Harris CL, Yan J (2007) Combined yeast {beta}-glucan and antitumor monoclonal antibody therapy requires C5a-mediated neutrophil chemotaxis via regulation of decay-accelerating factor CD55. Cancer Res 67:7421–7430PubMedCrossRef
111.
go back to reference Liu J, Gunn L, Hansen R, Yan J (2009) Combined yeast-derived beta-glucan with anti-tumor monoclonal antibody for cancer immunotherapy. Exp Mol Pathol 86:208–214PubMedCrossRef Liu J, Gunn L, Hansen R, Yan J (2009) Combined yeast-derived beta-glucan with anti-tumor monoclonal antibody for cancer immunotherapy. Exp Mol Pathol 86:208–214PubMedCrossRef
112.
go back to reference O’Connell J, O’Sullivan GC, Collins JK, Shanahan F (1996) The Fas counterattack: Fas-mediated T cell killing by colon cancer cells expressing Fas ligand. J Exp Med 184:1075–1082PubMedCrossRef O’Connell J, O’Sullivan GC, Collins JK, Shanahan F (1996) The Fas counterattack: Fas-mediated T cell killing by colon cancer cells expressing Fas ligand. J Exp Med 184:1075–1082PubMedCrossRef
113.
go back to reference Seino K, Kayagaki N, Okumura K, Yagita H (1997) Antitumor effect of locally produced CD95 ligand. Nat Med 3:165–170PubMedCrossRef Seino K, Kayagaki N, Okumura K, Yagita H (1997) Antitumor effect of locally produced CD95 ligand. Nat Med 3:165–170PubMedCrossRef
114.
go back to reference Shimizu M, Fontana A, Takeda Y, Yagita H, Yoshimoto T, Matsuzawa A (1999) Induction of antitumor immunity with Fas/APO-1 ligand (CD95L)-transfected neuroblastoma neuro-2a cells. J Immunol 162:7350–7357PubMed Shimizu M, Fontana A, Takeda Y, Yagita H, Yoshimoto T, Matsuzawa A (1999) Induction of antitumor immunity with Fas/APO-1 ligand (CD95L)-transfected neuroblastoma neuro-2a cells. J Immunol 162:7350–7357PubMed
115.
go back to reference Igney FH, Behrens CK, Krammer PH (2005) CD95L mediates tumor counterattack in vitro but induces neutrophil-independent tumor rejection in vivo. Int J Cancer 113:78–87PubMedCrossRef Igney FH, Behrens CK, Krammer PH (2005) CD95L mediates tumor counterattack in vitro but induces neutrophil-independent tumor rejection in vivo. Int J Cancer 113:78–87PubMedCrossRef
116.
go back to reference Dupont PJ, Warrens AN (2007) Fas ligand exerts its pro-inflammatory effects via neutrophil recruitment but not activation. Immunology 120:133–139PubMedCrossRef Dupont PJ, Warrens AN (2007) Fas ligand exerts its pro-inflammatory effects via neutrophil recruitment but not activation. Immunology 120:133–139PubMedCrossRef
117.
go back to reference Hohlbaum AM, Gregory MS, Ju ST, Marshak-Rothstein A (2001) Fas ligand engagement of resident peritoneal macrophages in vivo induces apoptosis and the production of neutrophil chemotactic factors. J Immunol 167:6217–6224PubMed Hohlbaum AM, Gregory MS, Ju ST, Marshak-Rothstein A (2001) Fas ligand engagement of resident peritoneal macrophages in vivo induces apoptosis and the production of neutrophil chemotactic factors. J Immunol 167:6217–6224PubMed
118.
go back to reference Wada A, Tada Y, Kawamura K, Takiguchi Y, Tatsumi K, Kuriyama T, Takenouchi T, Wang J, Tagawa M (2007) The effects of FasL on inflammation and tumor survival are dependent on its expression levels. Cancer Gene Ther 14:262–267PubMedCrossRef Wada A, Tada Y, Kawamura K, Takiguchi Y, Tatsumi K, Kuriyama T, Takenouchi T, Wang J, Tagawa M (2007) The effects of FasL on inflammation and tumor survival are dependent on its expression levels. Cancer Gene Ther 14:262–267PubMedCrossRef
119.
go back to reference Musiani P, Allione A, Modica A, Lollini PL, Giovarelli M, Cavallo F, Belardelli F, Forni G, Modesti A (1996) Role of neutrophils and lymphocytes in inhibition of a mouse mammary adenocarcinoma engineered to release IL-2, IL-4, IL-7, IL-10, IFN-alpha, IFN-gamma, and TNF-alpha. Lab Invest 74:146–157PubMed Musiani P, Allione A, Modica A, Lollini PL, Giovarelli M, Cavallo F, Belardelli F, Forni G, Modesti A (1996) Role of neutrophils and lymphocytes in inhibition of a mouse mammary adenocarcinoma engineered to release IL-2, IL-4, IL-7, IL-10, IFN-alpha, IFN-gamma, and TNF-alpha. Lab Invest 74:146–157PubMed
120.
go back to reference Stoppacciaro A, Melani C, Parenza M, Mastracchio A, Bassi C, Baroni C, Parmiani G, Colombo MP (1993) Regression of an established tumor genetically modified to release granulocyte colony-stimulating factor requires granulocyte-T cell cooperation and T cell-produced interferon gamma. J Exp Med 178:151–161PubMedCrossRef Stoppacciaro A, Melani C, Parenza M, Mastracchio A, Bassi C, Baroni C, Parmiani G, Colombo MP (1993) Regression of an established tumor genetically modified to release granulocyte colony-stimulating factor requires granulocyte-T cell cooperation and T cell-produced interferon gamma. J Exp Med 178:151–161PubMedCrossRef
121.
go back to reference Stoppacciaro A, Forni G, Colombo MP (1994) Different tumours, transduced with different cytokine genes as G-CSF and IL-2, show inhibition of tumour take through neutrophil activation but differ in T cell functions. Folia Biol (Praha) 40:89–99 Stoppacciaro A, Forni G, Colombo MP (1994) Different tumours, transduced with different cytokine genes as G-CSF and IL-2, show inhibition of tumour take through neutrophil activation but differ in T cell functions. Folia Biol (Praha) 40:89–99
122.
go back to reference Fridlender ZG, Albelda SM (2012) Tumor-associated neutrophils: friend or foe? Carcinogenesis 33:949–955PubMedCrossRef Fridlender ZG, Albelda SM (2012) Tumor-associated neutrophils: friend or foe? Carcinogenesis 33:949–955PubMedCrossRef
123.
go back to reference Scapini P, Nesi L, Morini M, Tanghetti E, Belleri M, Noonan D, Presta M, Albini A, Cassatella MA (2002) Generation of biologically active angiostatin kringle 1-3 by activated human neutrophils. J Immunol 168:5798–5804PubMed Scapini P, Nesi L, Morini M, Tanghetti E, Belleri M, Noonan D, Presta M, Albini A, Cassatella MA (2002) Generation of biologically active angiostatin kringle 1-3 by activated human neutrophils. J Immunol 168:5798–5804PubMed
124.
go back to reference Granot Z, Henke E, Comen EA, King TA, Norton L, Benezra R (2011) Tumor entrained neutrophils inhibit seeding in the premetastatic lung. Cancer Cell 20:300–314PubMedCrossRef Granot Z, Henke E, Comen EA, King TA, Norton L, Benezra R (2011) Tumor entrained neutrophils inhibit seeding in the premetastatic lung. Cancer Cell 20:300–314PubMedCrossRef
125.
go back to reference Lopez-Lago MA, Posner S, Thodima VJ, Molina AM, Motzer RJ, Chaganti RS (2012) Neutrophil chemokines secreted by tumor cells mount a lung antimetastatic response during renal cell carcinoma progression. Oncogene. doi:10.1038/onc.2012.201 [Epub ahead of print] Lopez-Lago MA, Posner S, Thodima VJ, Molina AM, Motzer RJ, Chaganti RS (2012) Neutrophil chemokines secreted by tumor cells mount a lung antimetastatic response during renal cell carcinoma progression. Oncogene. doi:10.​1038/​onc.​2012.​201 [Epub ahead of print]
Metadata
Title
Protumor and antitumor functions of neutrophil granulocytes
Authors
Sven Brandau
Claudia A. Dumitru
Stephan Lang
Publication date
01-03-2013
Publisher
Springer-Verlag
Published in
Seminars in Immunopathology / Issue 2/2013
Print ISSN: 1863-2297
Electronic ISSN: 1863-2300
DOI
https://doi.org/10.1007/s00281-012-0344-6

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