Cancer-promoting mechanisms of tumor-associated neutrophils

American Journal of Surgery

Volumn 214, Issue 5, 2017, Pages 938-944

  Hurt, Brian ^a   Schulick, Richard ^a   Edil, Barish ^a   El Kasmi, Karim C ^b   Barnett, Carlton ^a  

^a UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^b Center for Cancer and Blood Disorders   (United States)

Author keywords

Chemokines; Cytokines; Immunomodulation; Metastasis; Tumor microenvironment; Tumor progression; Tumor associated neutrophils

Indexed keywords

ARGINASE 1; GELATINASE B; INTERCELLULAR ADHESION MOLECULE 1; LEUKOCYTE ELASTASE; SCATTER FACTOR; VASCULOTROPIN;

ADVANCED CANCER; CANCER DIAGNOSIS; CANCER INHIBITION; CD8+ T LYMPHOCYTE; CELL FUNCTION; CELL MEMBRANE; CELL PROLIFERATION; CLINICAL ASSESSMENT; CYTOKINE RELEASE; DISTANT METASTASIS; EXTRACELLULAR MATRIX; HUMAN; MULTIMODALITY CANCER THERAPY; NEUTROPENIA; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; REVIEW; SIGNAL TRANSDUCTION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR ASSOCIATED NEUTROPHIL; TUMOR GROWTH; TUMOR IMMUNITY; TUMOR INVASION; TUMOR MICROENVIRONMENT; TUMOR PROMOTION; TUMOR VASCULARIZATION; UPREGULATION; DISEASE EXACERBATION; IMMUNOLOGY; NEOPLASM; NEUTROPHIL; PATHOLOGY; PHYSIOLOGY;

DISEASE PROGRESSION; HUMANS; NEOPLASMS; NEUTROPHILS; TUMOR MICROENVIRONMENT;

EID: 85027708729     PISSN: 00029610     EISSN: 18791883     Source Type: Journal    
DOI: 10.1016/j.amjsurg.2017.08.003     Document Type: Review

References (75)

1. Pietras, K., Östman, A., Hallmarks of cancer: interactions with the tumor stroma. Exp Cell Res 316:8 (2010), 1324–1331.
2. Ilkovitch, D., Lopez, D.M., The liver is a site for tumor-induced myeloid-derived suppressor cell accumulation and immunosuppression. Cancer Res 69:13 (2009), 5514–5521, 10.1158/0008-5472.CAN-08-4625.
3. Diaz-Montero, C.M., Salem, M.L., Nishimura, M.I., Garrett-Mayer, E., Cole, D.J., Montero, A.J., Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin-cyclophosphamide chemotherapy. Cancer Immunol Immunother 58:1 (2009), 49–59, 10.1007/s00262-008-0523-4.
4. Sionov, R.V., Fridlender, Z.G., Granot, Z., The multifaceted roles neutrophils play in the tumor microenvironment. Cancer Microenviron 8:3 (2015), 125–158.
5. Swierczak, A., Mouchemore, K.A., Hamilton, J.A., Anderson, R.L., Neutrophils: important contributors to tumor progression and metastasis. Cancer Metastasis Rev 34:4 (2015), 735–751.
6. Wang, S., Liu, Z., Wang, L., Zhang, X., NF-kappaB signaling pathway, inflammation and colorectal cancer. Cell Mol Immunol 6:5 (2009), 327–334, 10.1038/cmi.2009.43.
7. Coussens, L.M., Werb, Z., Inflammation and cancer. Nature 420:6917 (2002), 860–867, 10.1038/nature01322.Inflammation.
8. Ben-Neriah, Y., Karin, M., Inflammation meets cancer, with NF-κB as the matchmaker. Nat Immunol 12:8 (2011), 715–723, 10.1038/ni.2060.
9. Gregory, A.D., Houghton, A.M., Tumor-associated neutrophils: new targets for cancer therapy. Cancer Res 71:7 (2011), 2411–2416.
10. Lechner, M.G., Liebertz, D.J., Epstein, A.L., Characterization of cytokine-induced myeloid-derived suppressor cells from normal human peripheral blood mononuclear cells. J Immunol 185:4 (2010), 2273–2284, 10.4049/jimmunol.1000901.
11. Serafini, P., Borrello, I., Bronte, V., Myeloid suppressor cells in cancer: recruitment, phenotype, properties, and mechanisms of immune suppression. Semin Cancer Biol 16:1 (2006), 53–65, 10.1016/j.semcancer.2005.07.005.
12. Ugel, S., Delpozzo, F., Desantis, G., et al. Therapeutic targeting of myeloid-derived suppressor cells. Curr Opin Pharmacol 9:4 (2009), 470–481, 10.1016/j.coph.2009.06.014.
13. Zea, A.H., Rodriguez, P.C., Atkins, M.B., et al. Arginase-producing myeloid suppressor cells in renal cell carcinoma patients: a mechanism of tumor evasion. Cancer Res 65:8 (2005), 3044–3048, 10.1158/0008-5472.CAN-04-4505.
14. Kusmartsev, S., Nagaraj, S., Gabrilovich, D.I., Tumor-associated CD8+ T cell tolerance induced by bone marrow-derived immature myeloid cells. J Immunol 175:7 (2005), 4583–4592 doi:175/7/4583 [pii].
15. Fridlender, Z.G., Sun, J., Mishalian, I., et al. Transcriptomic analysis comparing tumor-associated neutrophils with granulocytic myeloid-derived suppressor cells and normal neutrophils. PLoS One, 7(2), 2012, 10.1371/journal.pone.0031524.
16. Fridlender, Z.G., Sun, J., Kim, S., et al. Polarization of tumor-associated neutrophil phenotype by TGF-beta: “N1” versus “N2” TAN. Cancer Cell 16:3 (2009), 183–194, 10.1016/j.ccr.2009.06.017.
17. Mishalian, I., Bayuh, R., Levy, L., Zolotarov, L., Michaeli, J., Fridlender, Z.G., Tumor-associated neutrophils (TAN) develop pro-tumorigenic properties during tumor progression. Cancer Immunol Immunother 62:11 (2013), 1745–1756.
18. Uribe-Querol, E., Rosales, C., Neutrophils in cancer: two sides of the same coin. J Immunol Res, 2015, 2015.
19. Liang, W., Ferrara, N., The complex role of neutrophils in tumor angiogenesis and metastasis. Cancer Immunol Res 4:2 (2016), 83–91, 10.1158/2326-6066.CIR-15-0313.
20. Sparmann, A., Bar-Sagi, D., Ras-induced interleukin-8 expression plays a critical role in tumor growth and angiogenesis. Cancer Cell 6:5 (2004), 447–458, 10.1016/j.ccr.2004.09.028.
21. Rodriguez, P.C., Zea, A.H., Culotta, K.S., Zabaleta, J., Ochoa, J.B., Ochoa, A.C., Regulation of T cell receptor CD3zeta chain expression by L-arginine. J Biol Chem 277:24 (2002), 21123–21129, 10.1074/jbc.M110675200.
22. Rotondo, R., Barisione, G., Mastracci, L., et al. IL-8 induces exocytosis of arginase 1 by neutrophil polymorphonuclears in nonsmall cell lung cancer. Int J Cancer 125:4 (2009), 887–893, 10.1002/ijc.24448.
23. Houghton, A.M., Rzymkiewicz, D.M., Ji, H., et al. Neutrophil elastase-mediated degradation of IRS-1 accelerates lung tumor growth. Nat Med 16:2 (2010), 219–223, 10.1038/nm.2084.
24. Yui, S., Osawa, Y., Ichisugi, T., Morimoto-Kamata, R., Neutrophil cathepsin G, but not elastase, induces aggregation of MCF-7 mammary carcinoma cells by a protease activity-dependent cell-oriented mechanism. Mediat Inflamm, 2014, 2014.
25. Gabrilovich, D.I., Bronte, V., Chen, S.-H., et al. The terminology issue for myeloid-derived suppressor cells. Cancer Res, 67(1), 2007, 425.
26. Vivanco, I., Sawyers, C.L., The phosphatidylinositol 3-Kinase AKT pathway in human cancer. Nat Rev Cancer 2:7 (2002), 489–501, 10.1038/nrc839.
27. Clavel, C., Polette, M., Doco, M., Binninger, I., Birembaut, P., Immunolocalization of matrix metallo-proteinases and their tissue inhibitor in human mammary pathology. Bull Cancer 79:3 (1992), 261–270.
28. Watanabe, H., Hattori, S., Katsuda, S., Nakanishi, I., Nagai, Y., Human neutrophil elastase: degradation of basement membrane components and immunolocalization in the tissue. J Biochem 108:5 (1990), 753–759.
29. Benson, D.D., Meng, X., Fullerton, D.A., et al. Activation state of stromal inflammatory cells in murine metastatic pancreatic adenocarcinoma. Am J Physiol Regul Integr Comp Physiol 302:9 (2012), R1067–R1075, 10.1152/ajpregu.00320.2011.
30. Dinney, C.P., Bielenberg, D.R., Perrotte, P., et al. Inhibition of basic fibroblast growth factor expression, angiogenesis, and growth of human bladder carcinoma in mice by systemic interferon-alpha administration. Cancer Res 58:4 (1998), 808–814 http://www.ncbi.nlm.nih.gov/pubmed/9485039.
31. Singh, R.K., Gutman, M., Bucana, C.D., Sanchez, R., Llansa, N., Fidler, I.J., Interferons alpha and beta down-regulate the expression of basic fibroblast growth factor in human carcinomas. Proc Natl Acad Sci U. S. A 92:10 (1995), 4562–4566, 10.1073/pnas.92.10.4562.
32. Bergers, G., Brekken, R., McMahon, G., et al. Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis. Nat Cell Biol 2:10 (2000), 737–744, 10.1038/35036374.
33. Jablonska, J., Leschner, S., Westphal, K., Lienenklaus, S., Weiss, S., Neutrophils responsive to endogenous IFN-beta regulate tumor angiogenesis and growth in a mouse tumor model. J Clin Invest 120:4 (2010), 1151–1164, 10.1172/JCI37223.
34. Queen, M.M., Ryan, R.E., Holzer, R.G., Keller-Peck, C.R., Jorcyk, C.L., Breast cancer cells stimulate neutrophils to produce Oncostatin M: potential implications for tumor progression. Cancer Res 65:19 (2005), 8896–8904, 10.1158/0008-5472.CAN-05-1734.
35. Jiang, W.G., Martin, T.A., Parr, C., Davies, G., Matsumoto, K., Nakamura, T., Hepatocyte growth factor, its receptor, and their potential value in cancer therapies. Crit Rev Oncol Hematol 53:1 (2005), 35–69, 10.1016/j.critrevonc.2004.09.004.
36. Liotta, L.A., Kleinerman, J., Saldel, G.M., The significance of hematogenous tumor cell clumps in the metastatic process. Cancer Res 36:3 (1976), 889–894.
37. Morimoto-Kamata, R., Mizoguchi, S., Ichisugi, T., Yui, S., Cathepsin G induces cell aggregation of human breast cancer MCF-7 cells via a 2-step mechanism: catalytic site-independent binding to the cell surface and enzymatic activity-dependent induction of the cell aggregation. Mediat Inflamm, 2012, 2012.
38. Huh, S.J., Liang, S., Sharma, A., Dong, C., Robertson, G.P., Transiently entrapped circulating tumor cells interact with neutrophils to facilitate lung metastasis development. Cancer Res 70:14 (2010), 6071–6082.
39. Roland, C.L., Harken, A.H., Sarr, M.G., Barnett, C.C., ICAM-1 expression determines malignant potential of cancer. Surg (United States) 141:6 (2007), 705–707, 10.1016/j.surg.2007.01.016.
40. Roland, C.L., Dineen, S.P., Toombs, J.E., et al. Tumor-derived intercellular adhesion molecule-1 mediates tumor-associated leukocyte infiltration in orthotopic pancreatic xenografts. Exp Biol Med 235:2 (2010), 263–270, 10.1258/ebm.2009.009215.
41. Crissman, J.D., Hatfield, J., Schaldenbrand, M., Sloane, B.F., Honn, K.V., Arrest and extravasation of B16 amelanotic melanoma in murine lungs. A light and electron microscopic study. Lab Invest 53:4 (1985), 470–478.
42. Mannori, G., Cecconi, O., Hanasaki, K., et al. Differential colon cancer cell adhesion to e-, P-, and L-selectin: role of mucin-type glycoproteins. Cancer Res 55:19 (1995), 4425–4431.
43. Strell, C., Lang, K., Niggemann, B., Zaenker, K.S., Entschladen, F., Neutrophil granulocytes promote the migratory activity of MDA-MB-468 human breast carcinoma cells via ICAM-1. Exp Cell Res 316:1 (2010), 138–148.
44. Spicer, J.D., McDonald, B., Cools-Lartigue, J.J., et al. Neutrophils promote liver metastasis via mac-1–Mediated interactions with circulating tumor cells. Cancer Res 72:16 (2012), 3919–3927.
45. Howard, K., Lo, K.K., Ao, L., et al. Intercellular adhesion molecule-1 mediates murine colon adenocarcinoma invasion. J Surg Res 187:1 (2014), 19–23.
46. Schmidt, H., Bastholt, L., Geertsen, P., et al. Elevated neutrophil and monocyte counts in peripheral blood are associated with poor survival in patients with metastatic melanoma: a prognostic model. Br J Cancer 93:3 (2005), 273–278.
47. Jensen, H.K., Donskov, F., Marcussen, N., Nordsmark, M., Lundbeck, F., Von Der Maase, H., Presence of intratumoral neutrophils is an independent prognostic factor in localized renal cell carcinoma. J Clin Oncol 27:28 (2009), 4709–4717, 10.1200/JCO.2008.18.9498.
48. Wislez, M., Rabbe, N., Marchal, J., et al. Hepatocyte growth factor production by neutrophils infiltrating bronchioloalveolar subtype pulmonary adenocarcinoma role in tumor progression and death. Cancer Res 63:6 (2003), 1405–1412.
49. Reid, M.D., Basturk, O., Thirabanjasak, D., et al. Tumor-infiltrating neutrophils in pancreatic neoplasia. Mod Pathol 24:12 (2011), 1612–1619.
50. Halazun, K.J., Hardy, M.A., Rana, A.A., et al. Negative impact of neutrophil-lymphocyte ratio on outcome after liver transplantation for hepatocellular carcinoma. Ann Surg 250:1 (2009), 141–151.
51. Trellakis, S., Bruderek, K., Dumitru, C.A., et al. Polymorphonuclear granulocytes in human head and neck cancer: enhanced inflammatory activity, modulation by cancer cells and expansion in advanced disease. Int J Cancer 129:9 (2011), 2183–2193.
52. Carus, A., Ladekarl, M., Hager, H., Nedergaard, B.S., Donskov, F., Tumour-associated CD66b+ neutrophil count is an independent prognostic factor for recurrence in localised cervical cancer. Br J Cancer 108:10 (2013), 2116–2122, 10.1038/bjc.2013.167.
53. Huang, S., Mills, L., Mian, B., et al. Fully humanized neutralizing antibodies to interleukin-8 (ABX-IL8) inhibit angiogenesis, tumor growth, and metastasis of human melanoma. Am J Pathol 161:1 (2002), 125–134, 10.1016/S0002-9440(10)64164-8.
54. Coffelt, S.B., Kersten, K., Doornebal, C.W., et al. IL-17-producing γδ T cells and neutrophils conspire to promote breast cancer metastasis. Nature 522:7556 (2015), 345–348, 10.1038/nature14282.
55. Arenberg, D.A., Kunkel, S.L., Polverini, P.J., Glass, M., Burdick, M.D., Strieter, R.M., Inhibition of interleukin-8 reduces tumorigenesis of human non-small cell lung cancer in SCID mice. J Clin Invest 97:12 (1996), 2792–2802, 10.1172/JCI118734.
56. Varney, M.L., Singh, S., Li, A., Mayer-Ezell, R., Bond, R., Singh, R.K., Small molecule antagonists for CXCR2 and CXCR1 inhibit human colon cancer liver metastases. Cancer Lett 300:2 (2011), 180–188, 10.1016/j.canlet.2010.10.004.
57. Li, A., Varney, M.L., Singh, R.K., Expression of interleukin 8 and its receptors in human colon carcinoma cells with different metastatic potentials. Clin Cancer Res 7:10 (2001), 3298–3304.
58. Goldberg, G.I., Renaissance of MMPs as therapeutic targets? Maybe. Structure 23:1 (2015), 6–7, 10.1016/j.str.2014.12.003.
59. Fridlender, Z.G., Albelda, S.M., Tumor-associated neutrophils: friend or foe?. Carcinogenesis 33:5 (2012), 949–955.
60. Giraudo, E., Inoue, M., Hanahan, D., An amino-bisphosphonate targets MMP-9-Expressing macrophages and angiogenesis to impair cervical carcinogenesis. J Clin Invest 114:5 (2004), 623–633, 10.1172/JCI200422087.
61. Pekarek, L.A., Starr, B.A., Toledano, A.Y., Schreiber, H., Inhibition of tumor growth by elimination of granulocytes. J Exp Med 181:1 (1995), 435–440, 10.1084/jem.181.1.435.
62. Tazawa, H., Okada, F., Kobayashi, T., et al. 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 163:6 (2003), 2221–2232, 10.1016/S0002-9440(10)63580-8.
63. Jain, R.K., Determinants of tumor blood flow: a review. Cancer Res 48:10 (1988), 2641–2658.
64. Kaushal, S., McElroy, M.K., Luiken, G.A., et al. Fluorophore-conjugated anti-CEA antibody for the intraoperative imaging of pancreatic and colorectal cancer. J Gastrointest Surg 12:11 (2008), 1938–1950, 10.1007/s11605-008-0581-0.
65. McElroy, M., Kaushal, S., Luiken, G.A., et al. Imaging of primary and metastatic pancreatic cancer using a fluorophore-conjugated anti-CA19-9 antibody for surgical navigation. World J Surg 32:6 (2008), 1057–1066, 10.1007/s00268-007-9452-1.
66. Bouvet, M., Tsuji, K., Yang, M., Jiang, P., Moossa, A.R., Hoffman, R.M., In vivo color-coded imaging of the interaction of colon cancer cells and splenocytes in the formation of liver metastases. Cancer Res 66:23 (2006), 11293–11297, 10.1158/0008-5472.CAN-06-2662.
67. Singletary, S.E., Surgical margins in patients with early-stage breast cancer treated with breast conservation therapy. Am J Surg 184:5 (2002), 383–393, 10.1016/S0002-9610(02)01012-7.
68. Sener, S.F., Fremgen, A., Menck, H.R., Winchester, D.P., Pancreatic cancer: a report of treatment and survival trends for 100,313 patients diagnosed from 1985–1995, using the National Cancer Database11No competing interests declared. J Am Coll Surg 189:1 (1999), 1–7, 10.1016/S1072-7515(99)00075-7.
69. Pawlik, T.M., Scoggins, C.R., Zorzi, D., et al. Effect of surgical margin status on survival and site of recurrence after hepatic resection for colorectal metastases. Ann Surg 241:5 (2005), 715–724, 10.1097/01.sla.0000160703.75808.7d.
70. Grossfeld, G.D., Chang, J.J., Broering, J.M., et al. Impact of positive surgical margins on prostate cancer recurrence and the use of secondary cancer treatment: data from the capsure database. J Urol 163:4 (2000), 1171–1177, 10.1016/S0022-5347(05)67716-6.
71. Dale, P.S., Souza, J.W., Brewer, D.A., Cryosurgical ablation of unresectable hepatic metastases. J Surg Oncol 68:4 (1998), 242–245, 10.1002/(SICI)1096-9098(199808)68:4<242::AID-JSO7>3.0.CO;2–4.
72. Eilber, F.R., Morton, D.L., Impaired immunologic reactivity and recurrence following cancer surgery. Cancer 25:2 (1970), 362–367, 10.1002/1097-0142(197002)25:2<362::AID-CNCR2820250213>3.0.CO;2-V.
73. Ishizuka, M., Nagata, H., Takagi, K., Horie, T., Kubota, K., Inflammation-based prognostic score is a novel predictor of postoperative outcome in patients with colorectal cancer. Ann Surg 246:6 (2007), 1047–1051, 10.1097/SLA.0b013e3181454171.
74. Kohl, B.A., Deutschman, C.S., The inflammatory response to surgery and trauma. Curr Opin Crit Care 12:4 (2006), 325–332, 10.1097/01.ccx.0000235210.85073.fc.
75. Weinberg, B.D., Patel, R.B., Wu, H., et al. Model simulation and experimental validation of intratumoral chemotherapy using multiple polymer implants. Med Biol Eng Comput 46:10 (2008), 1039–1049, 10.1007/s11517-008-0354-7.