Neutrophils and granulocytic myeloid-derived suppressor cells: immunophenotyping, cell biology and clinical relevance in human oncology (original) (raw)
References
Balkwill FR, Mantovani A (2012) Cancer-related inflammation: common themes and therapeutic opportunities. Semin Cancer Biol 22:33–40 ArticlePubMedCAS Google Scholar
Donskov F, von der Maase H (2006) Impact of immune parameters on long-term survival in metastatic renal cell carcinoma. J Clin Oncol 24:1997–2005 ArticlePubMed Google Scholar
Schmidt H, Suciu S, Punt CJ, Gore M, Kruit W, Patel P, Lienard D, von der Maase H, Eggermont AM, Keilholz U (2007) Pretreatment levels of peripheral neutrophils and leukocytes as independent predictors of overall survival in patients with American Joint Committee on Cancer Stage IV Melanoma: results of the EORTC 18951 Biochemotherapy Trial. J Clin Oncol 25:1562–1569 ArticlePubMedCAS Google Scholar
Teramukai S, Kitano T, Kishida Y, Kawahara M, Kubota K, Komuta K, Minato K, Mio T, Fujita Y, Yonei T, Nakano K, Tsuboi M, Shibata K, Furuse K, Fukushima M (2009) Pretreatment neutrophil count as an independent prognostic factor in advanced non-small-cell lung cancer: an analysis of Japan Multinational Trial Organisation LC00-03. Eur J Cancer 45:1950–1958 ArticlePubMed Google Scholar
Houghton AM, Rzymkiewicz DM, Ji H, Gregory AD, Egea EE, Metz HE, Stolz DB, Land SR, Marconcini LA, Kliment CR, Jenkins KM, Beaulieu KA, Mouded M, Frank SJ, Wong KK, Shapiro SD (2010) Neutrophil elastase-mediated degradation of IRS-1 accelerates lung tumor growth. Nat Med 16:219–223 ArticlePubMedCAS Google Scholar
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 54:948–955 ArticlePubMedCAS Google Scholar
Condamine T, Gabrilovich DI (2011) Molecular mechanisms regulating myeloid-derived suppressor cell differentiation and function. Trends Immunol 32:19–25 ArticlePubMedCAS Google Scholar
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 166:678–689 PubMedCAS Google Scholar
Garrity T, Pandit R, Wright MA, Benefield J, Keni S, Young MR (1997) Increased presence of CD34 + cells in the peripheral blood of head and neck cancer patients and their differentiation into dendritic cells. Int J Cancer 73:663–669 ArticlePubMedCAS Google Scholar
Rodriguez PC, Ernstoff MS, Hernandez C, Atkins M, Zabaleta J, Sierra R, Ochoa AC (2009) Arginase I-producing myeloid-derived suppressor cells in renal cell carcinoma are a subpopulation of activated granulocytes. Cancer Res 69:1553–1560 ArticlePubMedCAS Google Scholar
Schmielau J, Finn OJ (2001) Activated granulocytes and granulocyte-derived hydrogen peroxide are the underlying mechanism of suppression of t-cell function in advanced cancer patients. Cancer Res 61:4756–4760 PubMedCAS Google Scholar
Youn JI, Nagaraj S, Collazo M, Gabrilovich DI (2008) Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J Immunol 181:5791–5802 PubMedCAS Google Scholar
Zhang X, Majlessi L, Deriaud E, Leclerc C, Lo-Man R (2009) Coactivation of Syk kinase and MyD88 adaptor protein pathways by bacteria promotes regulatory properties of neutrophils. Immunity 31:761–771 ArticlePubMedCAS Google Scholar
Davey MS, Tamassia N, Rossato M, Bazzoni F, Calzetti F, Bruderek K, Sironi M, Zimmer L, Bottazzi B, Mantovani A, Brandau S, Moser B, Eberl M, Cassatella MA (2011) Failure to detect production of IL-10 by activated human neutrophils. Nat Immunol 12:1017–1018 ArticlePubMedCAS Google Scholar
Reglier H, Arce-Vicioso M, Fay M, Gougerot-Pocidalo MA, Chollet-Martin S (1998) Lack of IL-10 and IL-13 production by human polymorphonuclear neutrophils. Cytokine 10:192–198 ArticlePubMedCAS Google Scholar
Smedman C, Gardlund B, Nihlmark K, Gille-Johnson P, Andersson J, Paulie S (2009) ELISpot analysis of LPS-stimulated leukocytes: human granulocytes selectively secrete IL-8, MIP-1beta and TNF-alpha. J Immunol Methods 346:1–8 ArticlePubMedCAS Google Scholar
Azab B, Bhatt VR, Phookan J, Murukutla S, Kohn N, Terjanian T, Widmann WD (2012) Usefulness of the neutrophil-to-lymphocyte ratio in predicting short- and long-term mortality in breast cancer patients. Ann Surg Oncol 19:217–224 ArticlePubMed Google Scholar
Cho H, Hur HW, Kim SW, Kim SH, Kim JH, Kim YT, Lee K (2009) Pre-treatment neutrophil to lymphocyte ratio is elevated in epithelial ovarian cancer and predicts survival after treatment. Cancer Immunol Immunother 58:15–23 ArticlePubMedCAS Google Scholar
Ding PR, An X, Zhang RX, Fang YJ, Li LR, Chen G, Wu XJ, Lu ZH, Lin JZ, Kong LH, Wan DS, Pan ZZ (2010) Elevated preoperative neutrophil to lymphocyte ratio predicts risk of recurrence following curative resection for stage IIA colon cancer. Int J Colorectal Dis 25:1427–1433 ArticlePubMed Google Scholar
Aliustaoglu M, Bilici A, Seker M, Dane F, Gocun M, Konya V, Ustaalioglu BB, Gumus M (2010) The association of pre-treatment peripheral blood markers with survival in patients with pancreatic cancer. Hepatogastroenterology 57:640–645 PubMed Google Scholar
An X, Ding PR, Wang FH, Jiang WQ, Li YH (2011) Elevated neutrophil to lymphocyte ratio predicts poor prognosis in nasopharyngeal carcinoma. Tumour Biol 32:317–324 ArticlePubMedCAS Google Scholar
Tavares-Murta BM, Mendonca MA, Duarte NL, da Silva JA, Mutao TS, Garcia CB, Murta EF (2010) Systemic leukocyte alterations are associated with invasive uterine cervical cancer. Int J Gynecol Cancer 20:1154–1159 ArticlePubMed Google Scholar
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 129:2183–2193 ArticlePubMedCAS Google Scholar
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 24:683–693 PubMedCAS Google Scholar
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 33:121–129 ArticlePubMedCAS Google Scholar
Tanaka F, Goto H, Yokosuka T, Yanagimachi M, Kajiwara R, Naruto T, Nishimaki S, Yokota S (2009) Suppressed neutrophil function in children with acute lymphoblastic leukemia. Int J Hematol 90:311–317 ArticlePubMed Google Scholar
Uehara M, Sato N (1994) Impaired ability of neutrophils to produce oxygen-derived free radicals in patients with chronic liver disease and hepatocellular carcinoma. Hepatology 20:326–330 ArticlePubMedCAS Google Scholar
Shirai R, Kadota J, Iida K, Kawakami K, Abe K, Yoshinaga M, Iwashita T, Matsubara Y, Oka M, Kohno S (1998) Immunological competence and nutritional status in patients with lung cancer. Lung 176:363–370 ArticlePubMedCAS Google Scholar
Kastelan Z, Lukac J, Derezic D, Pasini J, Kusic Z, Sosic H, Kastelan M (2003) Lymphocyte subsets, lymphocyte reactivity to mitogens, NK cell activity and neutrophil and monocyte phagocytic functions in patients with bladder carcinoma. Anticancer Res 23:5185–5189 PubMed Google Scholar
Jablonska E, Piotrowski L, Kiluk M, Jablonski J, Grabowska Z, Markiewicz W (2001) Effect of IL-15 on the secretion of IL-1beta, IL-1Ra and sIL-1RII by PMN from cancer patients. Cytokine 16:173–177 ArticlePubMedCAS Google Scholar
Jablonska E, Puzewska W, Grabowska Z, Jablonski J, Talarek L (2005) VEGF, IL-18 and NO production by neutrophils and their serum levels in patients with oral cavity cancer. Cytokine 30:93–99 ArticlePubMedCAS Google Scholar
Jablonska E, Jablonski J, Marcinczyk M, Grabowska Z, Piotrowski L (2008) The release of soluble forms of TRAIL and DR5 by neutrophils of oral cavity cancer patients. Folia Histochem Cytobiol 46:177–183 ArticlePubMedCAS Google Scholar
Garley M, Jablonska E, Grabowska SZ, Piotrowski L (2009) IL-17 family cytokines in neutrophils of patients with oral epithelial squamous cell carcinoma. Neoplasma 56:96–100 ArticlePubMedCAS Google Scholar
Jablonska E, Garley M, Jablonski J (2009) The expressions of intrinsic and extrinsic apoptotic pathway proteins in neutrophils of oral cavity cancer patients: a preliminary study. Arch Immunol Ther Exp (Warsz) 57:229–234 ArticleCAS Google Scholar
De Santo C, Arscott R, Booth S, Karydis I, Jones M, Asher R, Salio M, Middleton M, Cerundolo V (2010) Invariant NKT cells modulate the suppressive activity of IL-10-secreting neutrophils differentiated with serum amyloid A. Nat Immunol 11:1039–1046 ArticlePubMed Google Scholar
Greten TF, Manns MP, Korangy F (2011) Myeloid derived suppressor cells in human diseases. Int Immunopharmacol 11:802–807 ArticlePubMedCAS Google Scholar
Filipazzi P, Valenti R, Huber V, Pilla L, Canese P, Iero M, Castelli C, Mariani L, Parmiani G, Rivoltini L (2007) Identification of a new subset of myeloid suppressor cells in peripheral blood of melanoma patients with modulation by a granulocyte-macrophage colony-stimulation factor-based antitumor vaccine. J Clin Oncol 25:2546–2553 ArticlePubMedCAS Google Scholar
Poschke I, Mougiakakos D, Hansson J, Masucci GV, Kiessling R (2010) Immature immunosuppressive CD14 + HLA-DR-/low cells in melanoma patients are Stat3hi and overexpress CD80, CD83, and DC-sign. Cancer Res 70:4335–4345 ArticlePubMedCAS Google Scholar
Hoechst B, Ormandy LA, Ballmaier M, Lehner F, Kruger C, Manns MP, Greten TF, Korangy F (2008) A new population of myeloid-derived suppressor cells in hepatocellular carcinoma patients induces CD4(+)CD25(+)Foxp3(+) T cells. Gastroenterology 135:234–243 ArticlePubMedCAS Google Scholar
van Cruijsen H, van der Veldt AA, Vroling L, Oosterhoff D, Broxterman HJ, Scheper RJ, Giaccone G, Haanen JB, van den Eertwegh AJ, Boven E, Hoekman K, de Gruijl TD (2008) Sunitinib-induced myeloid lineage redistribution in renal cell cancer patients: CD1c + dendritic cell frequency predicts progression-free survival. Clin Cancer Res 14:5884–5892 ArticlePubMed Google Scholar
Vuk-Pavlovic S, Bulur PA, Lin Y, Qin R, Szumlanski CL, Zhao X, Dietz AB (2010) Immunosuppressive CD14 + HLA-DRlow/- monocytes in prostate cancer. Prostate 70:443–455 PubMedCAS Google Scholar
Brimnes MK, Vangsted AJ, Knudsen LM, Gimsing P, Gang AO, Johnsen HE, Svane IM (2010) Increased level of both CD4 + FOXP3 + regulatory T cells and CD14 + HLA-DR/low myeloid-derived suppressor cells and decreased level of dendritic cells in patients with multiple myeloma. Scand J Immunol 72:540–547 ArticlePubMedCAS Google Scholar
Yuan XK, Zhao XK, Xia YC, Zhu X, Xiao P (2011) Increased circulating immunosuppressive CD14(+)HLA-DR(-/low) cells correlate with clinical cancer stage and pathological grade in patients with bladder carcinoma. J Int Med Res 39:1381–1391 PubMedCAS Google Scholar
Mundy-Bosse BL, Young GS, Bauer T, Binkley E, Bloomston M, Bill MA, Bekaii-Saab T, Carson WE III, Lesinski GB (2011) Distinct myeloid suppressor cell subsets correlate with plasma IL-6 and IL-10 and reduced interferon-alpha signaling in CD4 T cells from patients with GI malignancy. Cancer Immunol Immunother 60:1269–1279 ArticlePubMedCAS Google Scholar
Ko JS, Zea AH, Rini BI, Ireland JL, Elson P, Cohen P, Golshayan A, Rayman PA, Wood L, Garcia J, Dreicer R, Bukowski R, Finke JH (2009) Sunitinib mediates reversal of myeloid-derived suppressor cell accumulation in renal cell carcinoma patients. Clin Cancer Res 15:2148–2157 ArticlePubMedCAS Google Scholar
Zea AH, Rodriguez PC, Atkins MB, Hernandez C, Signoretti S, Zabaleta J, McDermott D, Quiceno D, Youmans A, O’Neill A, Mier J, Ochoa AC (2005) Arginase-producing myeloid suppressor cells in renal cell carcinoma patients: a mechanism of tumor evasion. Cancer Res 65:3044–3048 PubMedCAS Google Scholar
Porembka MR, Mitchem JB, Belt BA, Hsieh CS, Lee HM, Herndon J, Gillanders WE, Linehan DC, Goedegebuure P (2012) Pancreatic adenocarcinoma induces bone marrow mobilization of myeloid-derived suppressor cells which promote primary tumor growth. Cancer Immunol Immunother. 2012 Jan 4 (Epub ahead of print)
Srivastava MK, Bosch JJ, Thompson JA, Ksander BR, Edelman MJ, Ostrand-Rosenberg S (2008) Lung cancer patients’ CD4(+) T cells are activated in vitro by MHC II cell-based vaccines despite the presence of myeloid-derived suppressor cells. Cancer Immunol Immunother 57:1493–1504 ArticlePubMedCAS Google Scholar
Liu CY, Wang YM, Wang CL, Feng PH, Ko HW, Liu YH, Wu YC, Chu Y, Chung FT, Kuo CH, Lee KY, Lin SM, Lin HC, Wang CH, Yu CT, Kuo HP (2010) Population alterations of L-arginase- and inducible nitric oxide synthase-expressed CD11b +/CD14/CD15 +/CD33 + myeloid-derived suppressor cells and CD8 + T lymphocytes in patients with advanced-stage non-small cell lung cancer. J Cancer ResClin Oncol 136:35–45 ArticleCAS Google Scholar
McKenna KC, Beatty KM, Bilonick RA, Schoenfield L, Lathrop KL, Singh AD (2009) Activated CD11b + CD15 + granulocytes increase in the blood of patients with uveal melanoma. Invest Ophthalmol Vis Sci 50:4295–4303 ArticlePubMed Google Scholar
Eruslanov E, Neuberger M, Daurkin I, Perrin GQ, Algood C, Dahm P, Rosser C, Vieweg J, Gilbert SM, Kusmartsev S (2012) Circulating and tumor-infiltrating myeloid cell subsets in patients with bladder cancer. Int J Cancer 130:1109–1119 ArticlePubMedCAS Google Scholar
Raychaudhuri B, Rayman P, Ireland J, Ko J, Rini B, Borden EC, Garcia J, Vogelbaum MA, Finke J (2011) Myeloid-derived suppressor cell accumulation and function in patients with newly diagnosed glioblastoma. Neuro Oncol 13:591–599 ArticlePubMed Google Scholar
Sippel TR, White J, Nag K, Tsvankin V, Klaassen M, Kleinschmidt-Demasters BK, Waziri A (2011) Neutrophil degranulation and immunosuppression in patients with GBM: restoration of cellular immune function by targeting arginase I. Clin Cancer Res 17:6992–7002 ArticlePubMedCAS Google Scholar
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 89:311–317 ArticlePubMedCAS Google Scholar
Gabitass RF, Annels NE, Stocken DD, Pandha HA, Middleton GW (2011) Elevated myeloid-derived suppressor cells in pancreatic, esophageal and gastric cancer are an independent prognostic factor and are associated with significant elevation of the Th2 cytokine interleukin-13. Cancer Immunol Immunother 60:1419–1430 ArticlePubMedCAS Google Scholar
Rodrigues JC, Gonzalez GC, Zhang L, Ibrahim G, Kelly JJ, Gustafson MP, Lin Y, Dietz AB, Forsyth PA, Yong VW, Parney IF (2010) Normal human monocytes exposed to glioma cells acquire myeloid-derived suppressor cell-like properties. Neuro Oncol 12:351–365 ArticlePubMedCAS Google Scholar
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 118:2254–2265 ArticlePubMedCAS Google Scholar
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 207:2439–2453 ArticlePubMedCAS Google Scholar
Daud AI, Mirza N, Lenox B, Andrews S, Urbas P, Gao GX, Lee JH, Sondak VK, Riker AI, Deconti RC, Gabrilovich D (2008) Phenotypic and functional analysis of dendritic cells and clinical outcome in patients with high-risk melanoma treated with adjuvant granulocyte macrophage colony-stimulating factor. J Clin Oncol 26:3235–3241 ArticlePubMedCAS Google Scholar
Diaz-Montero CM, Salem ML, Nishimura MI, Garrett-Mayer E, Cole DJ, Montero AJ (2009) Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin-cyclophosphamide chemotherapy. Cancer Immunol Immunother 58:49–59 ArticlePubMedCAS Google Scholar
Kusmartsev S, Su Z, Heiser A, Dannull J, Eruslanov E, Kubler H, Yancey D, Dahm P, Vieweg J (2008) Reversal of myeloid cell-mediated immunosuppression in patients with metastatic renal cell carcinoma. Clin Cancer Res 14:8270–8278 ArticlePubMedCAS Google Scholar
Mirza N, Fishman M, Fricke I, Dunn M, Neuger AM, Frost TJ, Lush RM, Antonia S, Gabrilovich DI (2006) All-trans-retinoic acid improves differentiation of myeloid cells and immune response in cancer patients. Cancer Res 66:9299–9307 ArticlePubMedCAS Google Scholar
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 7:31524 Article Google Scholar
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 91:167–181 ArticlePubMedCAS Google Scholar
Mandruzzato S, Solito S, Falisi E, Francescato S, Chiarion-Sileni V, Mocellin S, Zanon A, Rossi CR, Nitti D, Bronte V, Zanovello P (2009) IL4Ralpha + myeloid-derived suppressor cell expansion in cancer patients. J. Immunol. 182:6562–6568 ArticlePubMedCAS Google Scholar
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 USA 103:12493–12498 ArticlePubMedCAS Google Scholar
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 120:1151–1164 ArticlePubMedCAS Google Scholar
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 179:1455–1470 ArticlePubMedCAS Google Scholar
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. 2012 Jan 18 (Epub ahead of print)
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 163:2221–2232 ArticlePubMedCAS Google Scholar
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 189:197–206 ArticlePubMedCAS Google Scholar
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 65:8896–8904 ArticlePubMedCAS Google Scholar
Hill EK, Sandbo S, Abramsohn E, Makelarski J, Wroblewski K, Wenrich ER, McCoy S, Temkin SM, Yamada SD, Lindau ST (2011) Assessing gynecologic and breast cancer survivors’ sexual health care needs. Cancer 117:2643–2651 ArticlePubMed Google Scholar
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 20:287–293 ArticlePubMedCAS Google Scholar
Ardi VC, Kupriyanova TA, Deryugina EI, Quigley JP (2007) Human neutrophils uniquely release TIMP-free MMP-9 to provide a potent catalytic stimulator of angiogenesis. Proc Natl Acad Sci USA 104:20262–20267 ArticlePubMedCAS Google Scholar
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 316:138–148 ArticlePubMedCAS Google Scholar
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 129:847–858 ArticlePubMedCAS Google Scholar
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 17:161–167 PubMedCAS Google Scholar
Giese A, Bjerkvig R, Berens ME, Westphal M (2003) Cost of migration: invasion of malignant gliomas and implications for treatment. J Clin Oncol 21:1624–1636 ArticlePubMedCAS Google Scholar
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 159:1613–1617 ArticlePubMedCAS Google Scholar
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 129:859–869 ArticlePubMedCAS Google Scholar
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 125:887–893 ArticlePubMedCAS Google Scholar
Wu Y, Zhao Q, Peng C, Sun L, Li XF, Kuang DM (2011) Neutrophils promote motility of cancer cells via a hyaluronan-mediated TLR4/PI3 K activation loop. J Pathol 225:438–447 ArticlePubMedCAS Google Scholar
Wislez M, Rabbe N, Marchal J, Milleron B, Crestani B, Mayaud C, Antoine M, Soler P, Cadranel J (2003) Hepatocyte growth factor production by neutrophils infiltrating bronchioloalveolar subtype pulmonary adenocarcinoma: role in tumor progression and death. Cancer Res 63:1405–1412 PubMedCAS Google Scholar
Shoenfeld Y, Tal A, Berliner S, Pinkhas J (1986) Leukocytosis in non hematological malignancies–a possible tumor-associated marker. J Cancer Res Clin Oncol 111:54–58 ArticlePubMedCAS Google Scholar
Halazun KJ, Aldoori A, Malik HZ, Al-Mukhtar A, Prasad KR, Toogood GJ, Lodge JP (2008) Elevated preoperative neutrophil to lymphocyte ratio predicts survival following hepatic resection for colorectal liver metastases. Eur J Surg Oncol 34:55–60 ArticlePubMedCAS Google Scholar
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 250:141–151 ArticlePubMed Google Scholar
Gomez D, Farid S, Malik HZ, Young AL, Toogood GJ, Lodge JP, Prasad KR (2008) Preoperative neutrophil-to-lymphocyte ratio as a prognostic predictor after curative resection for hepatocellular carcinoma. World J Surg 32:1757–1762 ArticlePubMedCAS Google Scholar
Shimada H, Takiguchi N, Kainuma O, Soda H, Ikeda A, Cho A, Miyazaki A, Gunji H, Yamamoto H, Nagata M (2010) High preoperative neutrophil-lymphocyte ratio predicts poor survival in patients with gastric cancer. Gastric Cancer 13:170–176 ArticlePubMed Google Scholar
Ohno Y, Nakashima J, Ohori M, Hatano T, Tachibana M (2010) Pretreatment neutrophil-to-lymphocyte ratio as an independent predictor of recurrence in patients with nonmetastatic renal cell carcinoma. J Urol 184:873–878 ArticlePubMed Google Scholar
Sharaiha RZ, Halazun KJ, Mirza F, Port JL, Lee PC, Neugut AI, Altorki NK, Abrams JA (2011) Elevated preoperative neutrophil:lymphocyte ratio as a predictor of postoperative disease recurrence in esophageal cancer. Ann Surg Oncol 18:3362–3369 ArticlePubMed Google Scholar
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 27:4709–4717 ArticlePubMed Google Scholar
Li YW, Qiu SJ, Fan J, Zhou J, Gao Q, Xiao YS, Xu YF (2011) Intratumoral neutrophils: a poor prognostic factor for hepatocellular carcinoma following resection. J Hepatol 54:497–505 ArticlePubMed Google Scholar
Ilie M, Hofman V, Ortholan C, Bonnetaud C, Coelle C, Mouroux J, Hofman P (2011) Predictive clinical outcome of the intratumoral CD66b-positive neutrophil- to-CD8-positive T-cell ratio in patients with resectable nonsmall cell lung cancer. Cancer 118:1726–1737 ArticlePubMed Google Scholar
Jensen TO, Schmidt H, Moller HJ, Donskov F, Hoyer M, Sjoegren P, Christensen IJ, Steiniche T (2011) Intratumoral neutrophils and plasmacytoid dendritic cells indicate poor prognosis and are associated with pSTAT3 expression in AJCC stage I/II melanoma. Cancer. 2011 Sep 22 (Epub ahead of print)
Fossati G, Ricevuti G, Edwards SW, Walker C, Dalton A, Rossi ML (1999) Neutrophil infiltration into human gliomas. Acta Neuropathol 98:349–354 ArticlePubMedCAS Google Scholar
Schwaller J, Schneider P, Mhawech-Fauceglia P, McKee T, Myit S, Matthes T, Tschopp J, Donze O, Le Gal FA, Huard B (2007) Neutrophil-derived APRIL concentrated in tumor lesions by proteoglycans correlates with human B-cell lymphoma aggressiveness. Blood 109:331–338 ArticlePubMedCAS Google Scholar