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Journal of Oncology
Volume 2013 (2013), Article ID 835956, 16 pages
http://dx.doi.org/10.1155/2013/835956
Review Article

Protumor Activities of the Immune Response: Insights in the Mechanisms of Immunological Shift, Oncotraining, and Oncopromotion

1Unidad de Investigación Médica en Enfermedades Infecciosas y Parasitarias (UIMEIP), Hospital de Pediatría Centro Médico Nacional Siglo XXI, Instituto Mexicano del Seguro Social, Avenida Cuauhtémoc 330, Colonia Doctores, 06725 Delegación Cuauhtémoc, DF, Mexico
2Programa de Doctorado en Ciencias Quimicobiológicas del Instituto Politécnico Nacional (IPN), Mexico
3Programa de Doctorado en Ciencias Biomédicas de la Universidad Autónoma de México (UNAM), Mexico

Received 20 December 2012; Accepted 25 January 2013

Academic Editor: Bruno Vincenzi

Copyright © 2013 G. K. Chimal-Ramírez et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. F. M. Burnet, “The concept of immunological surveillance,” Progress in Experimental Tumor Research, vol. 13, pp. 1–27, 1970. View at Google Scholar · View at Scopus
  2. L. Thomas, “On immunosurveillance in human cancer,” The Yale Journal of Biology and Medicine, vol. 55, no. 3-4, pp. 329–333, 1982. View at Google Scholar · View at Scopus
  3. F. R. Balkwill and A. Mantovani, “Cancer-related inflammation: common themes and therapeutic opportunities,” Seminars in Cancer Biology, vol. 22, no. 1, pp. 33–40, 2012. View at Publisher · View at Google Scholar
  4. D. G. DeNardo, P. Andreu, and L. M. Coussens, “Interactions between lymphocytes and myeloid cells regulate pro-versus anti-tumor immunity,” Cancer and Metastasis Reviews, vol. 29, no. 2, pp. 309–316, 2010. View at Publisher · View at Google Scholar · View at Scopus
  5. V. Shankaran, H. Ikeda, A. T. Bruce et al., “IFNγ, and lymphocytes prevent primary tumour development and shape tumour immunogenicity,” Nature, vol. 410, no. 6832, pp. 1107–1111, 2001. View at Publisher · View at Google Scholar · View at Scopus
  6. D. Ribatti and E. Crivellato, “Mast cells, angiogenesis and cancer,” Advances in Experimental Medicine and Biology, vol. 716, pp. 270–288, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. R. Kokenyesi, “Ovarian carcinoma cells synthesize both chondroitin sulfate and heparan sulfate cell surface proteoglycans that mediate cell adhesion to interstitial matrix,” Journal of Cellular Biochemistry, vol. 83, no. 2, pp. 259–270, 2001. View at Publisher · View at Google Scholar · View at Scopus
  8. S. A. Oldford, I. D. Haidl, M. A. Howatt, C. A. Leiva, B. Johnston, and J. S. Marshall, “A critical role for mast cells and mast cell-derived IL-6 in TLR2-mediated inhibition of tumor growth,” Journal of Immunology, vol. 185, no. 11, pp. 7067–7076, 2010. View at Publisher · View at Google Scholar · View at Scopus
  9. S. Ch'ng, R. A. Wallis, L. Yuan, P. F. Davis, and S. T. Tan, “Mast cells and cutaneous malignancies,” Modern Pathology, vol. 19, no. 1, pp. 149–159, 2006. View at Publisher · View at Google Scholar · View at Scopus
  10. S. Maltby, K. Khazaie, and K. M. McNagny, “Mast cells in tumor growth: angiogenesis, tissue remodelling and immune-modulation,” Biochimica et Biophysica Acta, vol. 1796, no. 1, pp. 19–26, 2009. View at Publisher · View at Google Scholar · View at Scopus
  11. F. Della Rovere, A. Granata, M. Monaco, and G. Basile, “Phagocytosis of cancer cells by mast cells in breast cancer,” Anticancer Research, vol. 29, no. 8, pp. 3157–3161, 2009. View at Google Scholar · View at Scopus
  12. C. T. N. Pham, “Neutrophil serine proteases: specific regulators of inflammation,” Nature Reviews Immunology, vol. 6, no. 7, pp. 541–550, 2006. View at Publisher · View at Google Scholar · View at Scopus
  13. P. Scapini, J. A. Lapinet-Vera, S. Gasperini, F. Calzetti, F. Bazzoni, and M. A. Cassatella, “The neutrophil as a cellular source of chemokines,” Immunological Reviews, vol. 177, pp. 195–203, 2000. View at Google Scholar · View at Scopus
  14. M. P. Colombo, L. Lombardi, A. Stoppacciaro et al., “Granulocyte colony-stimulating factor (G-CSF) gene transduction in murine adenocarcinoma drives neutrophil-mediated tumor inhibition in vivo: neutrophils discriminate between G-CSF-producing and G-CSF-nonproducing tumor cells,” Journal of Immunology, vol. 149, no. 1, pp. 113–119, 1992. View at Google Scholar · View at Scopus
  15. E. Di Carlo, G. Forni, P. Lollini, M. P. Colombo, A. Modesti, and P. Musiani, “The intriguing role of polymorphonuclear neutrophils in antitumor reactions,” Blood, vol. 97, no. 2, pp. 339–345, 2001. View at Publisher · View at Google Scholar · View at Scopus
  16. D. R. Welch, D. J. Schissel, R. P. Howrey, and P. A. Aeed, “Tumor-elicited polymorphonuclear cells, in contrast to 'normal' circulating polymorphonuclear cells, stimulate invasive and metastatic potentials of rat mammary adenocarcinoma cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 86, no. 15, pp. 5859–5863, 1989. View at Google Scholar · View at Scopus
  17. Z. G. Fridlender, J. Sun, S. Kim et al., “Polarization of tumor-associated neutrophil phenotype by TGF-beta: “N1” versus “N2” TAN,” Cancer Cell, vol. 16, pp. 183–194, 2009. View at Google Scholar
  18. A. D. Gregory and A. M. Houghton, “Tumor-associated neutrophils: new targets for cancer therapy,” Cancer Research, vol. 71, no. 7, pp. 2411–2416, 2011. View at Publisher · View at Google Scholar · View at Scopus
  19. D. Rittmeyer and A. Lorentz, “Relationship between allergy and cancer: an overview,” International Archives of Allergy and Immunology, vol. 159, pp. 216–225, 2012. View at Publisher · View at Google Scholar
  20. M. C. Turner, “Epidemiology: allergy history, IgE, and cancer,” Cancer Immunology, Immunotherapy, vol. 61, no. 9, pp. 1493–1510, 2011. View at Publisher · View at Google Scholar
  21. F. Geissmann, M. G. Manz, S. Jung, M. H. Sieweke, M. Merad, and K. Ley, “Development of monocytes, macrophages, and dendritic cells,” Science, vol. 327, no. 5966, pp. 656–661, 2010. View at Publisher · View at Google Scholar · View at Scopus
  22. K. Karre, H. G. Ljunggren, G. Piontek, and R. Kiessling, “Selective rejection of H-2-deficient lymphoma variants suggests alternative immune defence strategy,” Nature, vol. 319, no. 6055, pp. 675–678, 1986. View at Google Scholar · View at Scopus
  23. D. H. Raulet, R. E. Vance, and C. W. McMahon, “Regulation of the natural killer cell receptor repertoire,” Annual Review of Immunology, vol. 19, pp. 291–330, 2001. View at Publisher · View at Google Scholar · View at Scopus
  24. I. Langers, V. M. Renoux, M. Thiry, P. Delvenne, and N. Jacobs, “Natural killer cells: role in local tumor growth and metastasis,” Biologics: Targets & Therapy, vol. 6, pp. 73–82, 2012. View at Google Scholar
  25. R. A. O'Connor, L. S. Taams, and S. M. Anderton, “Translational mini-review series on Th17 cells: CD4+ T helper cells: functional plasticity and differential sensitivity to regulatory T cell-mediated regulation,” Clinical and Experimental Immunology, vol. 159, no. 2, pp. 137–147, 2010. View at Publisher · View at Google Scholar · View at Scopus
  26. J. B. Wing and S. Sakaguchi, “Multiple treg suppressive modules and their adaptability,” Frontiers in Immunology, vol. 3, p. 178, 2012. View at Google Scholar
  27. C. T. Weaver, L. E. Harrington, P. R. Mangan, M. Gavrieli, and K. M. Murphy, “Th17: an effector CD4 T cell lineage with regulatory T cell ties,” Immunity, vol. 24, no. 6, pp. 677–688, 2006. View at Publisher · View at Google Scholar · View at Scopus
  28. J. R. Whitfield and L. Soucek, “Tumor microenvironment: becoming sick of Myc,” Cellular and Molecular Life Sciences, vol. 69, pp. 931–934, 2012. View at Google Scholar
  29. E. Fuentes-Pananá, M. Camorlinga-Ponce, and C. Maldonado-Bernal, “Infection, inflammation and gastric cancer,” Salud Publica de Mexico, vol. 51, no. 5, pp. 427–433, 2009. View at Google Scholar · View at Scopus
  30. F. Colotta, P. Allavena, A. Sica, C. Garlanda, and A. Mantovani, “Cancer-related inflammation, the seventh hallmark of cancer: links to genetic instability,” Carcinogenesis, vol. 30, no. 7, pp. 1073–1081, 2009. View at Publisher · View at Google Scholar · View at Scopus
  31. T. Fiaschi and P. Chiarugi, “Oxidative stress, tumor microenvironment, and metabolic reprogramming: a diabolic liaison,” International Journal of Cell Biology, vol. 2012, Article ID 762825, 8 pages, 2012. View at Publisher · View at Google Scholar
  32. A. Harada, N. Sekido, T. Akahoshi, T. Wada, N. Mukaida, and K. Matsushima, “Essential involvement of interleukin-8 (IL-8) in acute inflammation,” Journal of Leukocyte Biology, vol. 56, no. 5, pp. 559–564, 1994. View at Google Scholar · View at Scopus
  33. M. Johansson, D. G. Denardo, and L. M. Coussens, “Polarized immune responses differentially regulate cancer development,” Immunological Reviews, vol. 222, no. 1, pp. 145–154, 2008. View at Publisher · View at Google Scholar · View at Scopus
  34. S. I. Grivennikov, F. R. Greten, and M. Karin, “Immunity, inflammation, and cancer,” Cell, vol. 140, no. 6, pp. 883–899, 2010. View at Publisher · View at Google Scholar · View at Scopus
  35. Q. Xu, L. Wang, H. Li et al., “Mesenchymal stem cells play a potential role in regulating the establishment and maintenance of epithelial-mesenchymal transition in MCF7 human breast cancer cells by paracrine and induced autocrine TGF-beta,” International Journal of Oncology, vol. 41, no. 3, 2012. View at Publisher · View at Google Scholar
  36. H. Wang, J. Wu, Y. Zhang et al., “Transforming growth factor beta-induced epithelial-mesenchymal transition increases cancer stem-like cells in the PANC-1 cell line,” Oncology Letters, vol. 3, pp. 229–233, 2012. View at Google Scholar
  37. K. Malinowsky, M. Raychaudhuri, T. Buchner et al., “Common protein biomarkers assessed by reverse phase protein arrays show considerable intratumoral heterogeneity in breast cancer tissues,” PloS One, vol. 7, Article ID e40285, 2012. View at Google Scholar
  38. R. Schillaci, P. Guzman, F. Cayrol et al., “Clinical relevance of ErbB-2/HER2 nuclear expression in breast cancer,” BMC Cancer, vol. 12, article 74, 2012. View at Publisher · View at Google Scholar
  39. J. Giannios and L. Ioannidou-Mouzaka, “Molecular aspects of breast and ovarian cancer,” European Journal of Gynaecological Oncology, vol. 18, no. 5, pp. 387–393, 1997. View at Google Scholar · View at Scopus
  40. E. A. Tindall, G. Severi, H. N. Hoang et al., “Interleukin-6 promoter variants, prostate cancer risk, and survival,” The Prostate, vol. 72, no. 16, pp. 1701–1707, 2012. View at Publisher · View at Google Scholar
  41. Y. Wang, L. Li, X. Guo et al., “Interleukin-6 signaling regulates anchorage-independent growth, proliferation, adhesion and invasion in human ovarian cancer cells,” Cytokine, vol. 59, pp. 228–236, 2012. View at Publisher · View at Google Scholar
  42. A. Mantovani and A. Sica, “Macrophages, innate immunity and cancer: balance, tolerance, and diversity,” Current Opinion in Immunology, vol. 22, no. 2, pp. 231–237, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. D. I. Gabrilovich, S. Ostrand-Rosenberg, and V. Bronte, “Coordinated regulation of myeloid cells by tumours,” Nature Reviews Immunology, vol. 12, pp. 253–268, 2012. View at Publisher · View at Google Scholar
  44. Y. Ben-Neriah and M. Karin, “Inflammation meets cancer, with NF-kappaB as the matchmaker,” Nature Immunology, vol. 12, pp. 715–723, 2011. View at Google Scholar
  45. F. R. Greten, L. Eckmann, T. F. Greten et al., “IKKβ links inflammation and tumorigenesis in a mouse model of colitis-associated cancer,” Cell, vol. 118, no. 3, pp. 285–296, 2004. View at Publisher · View at Google Scholar · View at Scopus
  46. R. Nehra, R. B. Riggins, A. N. Shajahan, A. Zwart, A. C. Crawford, and R. Clarke, “BCL2 and CASP8 regulation by NF-κB differentially affect mitochondrial function and cell fate in antiestrogen-sensitive and -resistant breast cancer cells,” The FASEB Journal, vol. 24, no. 6, pp. 2040–2055, 2010. View at Publisher · View at Google Scholar · View at Scopus
  47. A. S. Baldwin, “Control of oncogenesis and cancer therapy resistance by the transcription factor NF-κB,” Journal of Clinical Investigation, vol. 107, no. 3, pp. 241–246, 2001. View at Google Scholar · View at Scopus
  48. K. Sheppard, K. M. Kinross, B. Solomon, R. B. Pearson, and W. A. Phillips, “Targeting PI3 kinase/AKT/mTOR signaling in cancer,” Critical Reviews in Oncogenesis, vol. 17, pp. 69–95, 2012. View at Google Scholar
  49. L. Trojan, D. Thomas, T. Knoll, R. Grobholz, P. Alken, and M. S. Michel, “Expression of pro-angiogenic growth factors VEGF, EGF and bFGF and their topographical relation to neovascularisation in prostate cancer,” Urological Research, vol. 32, no. 2, pp. 97–103, 2004. View at Publisher · View at Google Scholar · View at Scopus
  50. C. W. Pugh and P. J. Ratcliffe, “Regulation of angiogenesis by hypoxia: role of the HIF system,” Nature Medicine, vol. 9, no. 6, pp. 677–684, 2003. View at Publisher · View at Google Scholar · View at Scopus
  51. K. Shen, L. Ji, C. Gong et al., “Notoginsenoside Ft1 promotes angiogenesis via HIF-1α mediated VEGF secretion and the regulation of PI3K/AKT and Raf/MEK/ERK signaling pathways,” Biochemical Pharmacology, vol. 84, no. 6, pp. 784–792, 2012. View at Publisher · View at Google Scholar
  52. D. J. Hicklin and L. M. Ellis, “Role of the vascular endothelial growth factor pathway in tumor growth and angiogenesis,” Journal of Clinical Oncology, vol. 23, no. 5, pp. 1011–1027, 2005. View at Publisher · View at Google Scholar · View at Scopus
  53. J. Wels, R. N. Kaplan, S. Rafii, and D. Lyden, “Migratory neighbors and distant invaders: tumor-associated niche cells,” Genes and Development, vol. 22, no. 5, pp. 559–574, 2008. View at Publisher · View at Google Scholar · View at Scopus
  54. T. B. Wang, Z. G. Chen, X. Q. Wei, B. Wei, and W. G. Dong, “Serum vascular endothelial growth factor-C and lymphoangiogenesis are associated with the lymph node metastasis and prognosis of patients with colorectal cancer,” ANZ Journal of Surgery, vol. 81, pp. 694–699, 2011. View at Publisher · View at Google Scholar
  55. L. J. Talbot, S. D. Bhattacharya, and P. C. Kuo, “Epithelial-mesenchymal transition, the tumor microenvironment, and metastatic behavior of epithelial malignancies,” International Journal of Biochemistry and Molecular Biology, vol. 3, pp. 117–136, 2012. View at Google Scholar
  56. N. P. Gunasinghe, A. Wells, E. W. Thompson, and H. J. Hugo, “Mesenchymal-epithelial transition (MET) as a mechanism for metastatic colonisation in breast cancer,” Cancer Metastasis Reviews, vol. 31, no. 3-4, pp. 469–478, 2012. View at Publisher · View at Google Scholar
  57. A. A. Onitilo, G. Aryal, and J. M. Engel, “Hereditary diffuse Gastric cancer: a family diagnosis and treatment,” Clinical Medicine & Research, 2012. View at Publisher · View at Google Scholar
  58. S. Masciari, N. Larsson, J. Senz et al., “Germline E-cadherin mutations in familial lobular breast cancer,” Journal of Medical Genetics, vol. 44, no. 11, pp. 726–731, 2007. View at Publisher · View at Google Scholar · View at Scopus
  59. F. Y. Huang, A. O. Chan, A. Rashid, D. K. Wong, C. H. Cho, and M. F. Yuen, “Helicobacter pylori induces promoter methylation of E-cadherin via interleukin-1β activation of nitric oxide production in gastric cancer cells,” Cancer, vol. 118, no. 20, pp. 4969–4980, 2012. View at Publisher · View at Google Scholar
  60. B. Hoy, T. Geppert, M. Boehm et al., “Distinct roles of secreted HtrA proteases from gram-negative pathogens in cleaving the junctional protein and tumor suppressor E-cadherin,” The Journal of Biological Chemistry, vol. 287, pp. 10115–10120, 2012. View at Publisher · View at Google Scholar
  61. N. Murata-Kamiya, Y. Kurashima, Y. Teishikata et al., “Helicobacter pylori CagA interacts with E-cadherin and deregulates the β-catenin signal that promotes intestinal transdifferentiation in gastric epithelial cells,” Oncogene, vol. 26, no. 32, pp. 4617–4626, 2007. View at Publisher · View at Google Scholar · View at Scopus
  62. H. Mutoh, S. Sakurai, K. Satoh et al., “Cdx1 induced intestinal metaplasia in the transgenic mouse stomach: comparative study with Cdx2 transgenic mice,” Gut, vol. 53, no. 10, pp. 1416–1423, 2004. View at Publisher · View at Google Scholar · View at Scopus
  63. Y. Saito, N. Murata-Kamiya, T. Hirayama, Y. Ohba, and M. Hatakeyama, “Conversion of Helicobacter pylori CagA from senescence inducer to oncogenic driver through polarity-dependent regulation of p21,” The Journal of Experimental Medicine, vol. 207, no. 10, pp. 2157–2174, 2010. View at Publisher · View at Google Scholar · View at Scopus
  64. F. Hussain, P. E. Morton, M. Snippe et al., “CAR modulates E-cadherin dynamics in the presence of adenovirus type 5,” PLoS One, vol. 6, no. 8, Article ID e23056, 2011. View at Publisher · View at Google Scholar · View at Scopus
  65. K. Matthews, C. M. Leong, L. Baxter et al., “Depletion of Langerhans cells in human papillomavirus type 16-infected skin is associated with E6-mediated down regulation of E-cadherin,” Journal of Virology, vol. 77, no. 15, pp. 8378–8385, 2003. View at Publisher · View at Google Scholar · View at Scopus
  66. J. O. Lee, H. J. Kwun, J. K. Jung, K. H. Choi, D. S. Min, and K. L. Jang, “Hepatitis B virus X protein represses E-cadherin expression via activation of DNA methyltransferase 1,” Oncogene, vol. 24, no. 44, pp. 6617–6625, 2005. View at Publisher · View at Google Scholar · View at Scopus
  67. J. M. Lee, S. Dedhar, R. Kalluri, and E. W. Thompson, “The epithelial-mesenchymal transition: new insights in signaling, development, and disease,” Journal of Cell Biology, vol. 172, no. 7, pp. 973–981, 2006. View at Publisher · View at Google Scholar · View at Scopus
  68. Y. Jing, Z. Han, S. Zhang, Y. Liu, and L. Wei, “Epithelial-Mesenchymal transition in tumor microenvironment,” Cell & Bioscience, vol. 1, article 29, 2011. View at Publisher · View at Google Scholar
  69. C. López-Otín and T. Hunter, “The regulatory crosstalk between kinases and proteases in cancer,” Nature Reviews Cancer, vol. 10, no. 4, pp. 278–292, 2010. View at Publisher · View at Google Scholar · View at Scopus
  70. S. D. Mason and J. A. Joyce, “Proteolytic networks in cancer,” Trends in Cell Biology, vol. 21, no. 4, pp. 228–237, 2011. View at Publisher · View at Google Scholar · View at Scopus
  71. G. Bergers, R. Brekken, G. McMahon et al., “Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis,” Nature Cell Biology, vol. 2, no. 10, pp. 737–744, 2000. View at Publisher · View at Google Scholar · View at Scopus
  72. B. C. Victor, A. Anbalagan, M. M. Mohamed, B. F. Sloane, and D. Cavallo-Medved, “Inhibition of cathepsin B activity attenuates extracellular matrix degradation and inflammatory breast cancer invasion,” Breast Cancer Research, vol. 13, article R115, 2011. View at Google Scholar
  73. M. J. Duffy, T. M. Maguire, E. W. McDermott, and N. O'Higgins, “Urokinase plasminogen activator: a prognostic marker in multiple types of cancer,” Journal of Surgical Oncology, vol. 71, pp. 130–135, 1999. View at Publisher · View at Google Scholar
  74. M. J. Duffy, “Urokinase-type plasminogen activator: a potent marker of metastatic potential in human cancers,” Biochemical Society Transactions, vol. 30, no. 2, pp. 207–210, 2002. View at Google Scholar · View at Scopus
  75. S. Jelisavac-Cosic, M. Sirotkovic-Skerlev, A. Kulic, J. Jakic-Razumovic, Z. Kovac, and D. Vrbanec, “Prognostic significance of urokinase-type plasminogen activator (uPA) and plasminogen activator inhibitor (PAI-1) in patients with primary invasive ductal breast carcinoma—a 7.5-year follow-up study,” Tumori, vol. 97, pp. 532–539, 2011. View at Google Scholar
  76. B. R. Whitley, D. Palmieri, C. D. Twerdi, and F. C. Church, “Expression of active plasminogen activator inhibitor-1 reduces cell migration and invasion in breast and gynecological cancer cells,” Experimental Cell Research, vol. 296, no. 2, pp. 151–162, 2004. View at Publisher · View at Google Scholar · View at Scopus
  77. V. Magdolen, A. Krüger, S. Sato et al., “Inhibition of the tumor-associated urokinase-type plasminogen activation system: effects of high-level synthesis of soluble urokinase receptor in ovarian and breast cancer cells in vitro and in vivo,” Recent Results in Cancer Research, vol. 162, pp. 43–63, 2003. View at Google Scholar · View at Scopus
  78. E. Giraudo, M. Inoue, and D. Hanahan, “An amino-bisphosphonate targets MMP-9—expressing macrophages and angiogenesis to impair cervical carcinogenesis,” Journal of Clinical Investigation, vol. 114, no. 5, pp. 623–633, 2004. View at Publisher · View at Google Scholar · View at Scopus
  79. L. M. Coussens, C. L. Tinkle, D. Hanahan, and Z. Werb, “MMP-9 supplied by bone marrow-derived cells contributes to skin carcinogenesis,” Cell, vol. 103, no. 3, pp. 481–490, 2000. View at Google Scholar · View at Scopus
  80. R. E. Coleman, “Bisphosphonates in breast cancer,” Annals of Oncology, vol. 16, no. 5, pp. 687–695, 2005. View at Publisher · View at Google Scholar · View at Scopus
  81. W. Tan, W. Zhang, A. Strasner et al., “Tumour-infiltrating regulatory T cells stimulate mammary cancermetastasis through RANKL-RANK signalling,” Nature, vol. 470, no. 7335, pp. 548–553, 2011. View at Publisher · View at Google Scholar · View at Scopus
  82. R. N. Kaplan, R. D. Riba, S. Zacharoulis et al., “VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche,” Nature, vol. 438, no. 7069, pp. 820–827, 2005. View at Publisher · View at Google Scholar · View at Scopus
  83. M. Shokeen, A. Zheleznyak, J. M. Wilson et al., “Molecular imaging of very late antigen-4 (alpha4beta1 integrin) in the premetastatic niche,” Journal of Nuclear Medicine, vol. 53, pp. 779–786, 2012. View at Google Scholar
  84. F. Bolat, F. Kayaselcuk, T. Z. Nursal, M. C. Yagmurdur, N. Bal, and B. Demirhan, “Microvessel density, VEGF expression, and tumor-associated macrophages in breast tumors: correlations with prognostic parameters,” Journal of Experimental and Clinical Cancer Research, vol. 25, no. 3, pp. 365–372, 2006. View at Google Scholar · View at Scopus
  85. S. Osinsky, L. Bubnovskaya, I. Ganusevich et al., “Hypoxia, tumour-associated macrophages, microvessel density, VEGF and matrix metalloproteinases in human gastric cancer: interaction and impact on survival,” Clinical and Translational Oncology, vol. 13, no. 2, pp. 133–138, 2011. View at Publisher · View at Google Scholar · View at Scopus
  86. K. E. de Visser, A. Eichten, and L. M. Coussens, “Paradoxical roles of the immune system during cancer development,” Nature Reviews Cancer, vol. 6, no. 1, pp. 24–37, 2006. View at Publisher · View at Google Scholar · View at Scopus
  87. A. Rabenhorst, M. Schlaak, L. C. Heukamp et al., “Mast cells play a protumorigenic role in primary cutaneous lymphoma,” Blood, vol. 120, no. 10, pp. 2042–2054, 2012. View at Publisher · View at Google Scholar
  88. S. J. Priceman, J. L. Sung, Z. Shaposhnik et al., “Targeting distinct tumor-infiltrating myeloid cells by inhibiting CSF-1 receptor: combating tumor evasion of antiangiogenic therapy,” Blood, vol. 115, no. 7, pp. 1461–1471, 2010. View at Publisher · View at Google Scholar · View at Scopus
  89. E. Y. Lin, A. V. Nguyen, R. G. Russell, and J. W. Pollard, “Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy,” The Journal of Experimental Medicine, vol. 193, no. 6, pp. 727–740, 2001. View at Publisher · View at Google Scholar · View at Scopus
  90. A. Patsialou, J. Wyckoff, Y. Wang, S. Goswami, E. R. Stanley, and J. S. Condeelis, “Invasion of human breast cancer cells in vivo requires both paracrine and autocrine loops involving the colony-stimulating factor-1 receptor,” Cancer Research, vol. 69, no. 24, pp. 9498–9506, 2009. View at Publisher · View at Google Scholar · View at Scopus
  91. S. Agarwal, G. V. Reddy, and P. Reddanna, “Eicosanoids in inflammation and cancer: the role of COX-2,” Expert Review of Clinical Immunology, vol. 5, no. 2, pp. 145–165, 2009. View at Publisher · View at Google Scholar · View at Scopus
  92. D. Wang and R. N. Dubois, “Eicosanoids and cancer,” Nature Reviews Cancer, vol. 10, no. 3, pp. 181–193, 2010. View at Publisher · View at Google Scholar · View at Scopus
  93. J. Cuzick, F. Otto, J. A. Baron et al., “Aspirin and non-steroidal anti-inflammatory drugs for cancer prevention: an international consensus statement,” The Lancet Oncology, vol. 10, no. 5, pp. 501–507, 2009. View at Publisher · View at Google Scholar · View at Scopus
  94. A. Ferrandez, E. Piazuelo, and A. Castells, “Aspirin and the prevention of colorectal cancer,” Best Practice & Research. Clinical Gastroenterology, vol. 26, no. 2, pp. 185–195, 2012. View at Publisher · View at Google Scholar
  95. J. Garaude, A. Kent, N. van Rooijen, and J. M. Blander, “Simultaneous targeting of toll- and nod-like receptors induces effective tumor-specific immune responses,” Science Translational Medicine, vol. 4, Article ID 120ra116, 2012. View at Google Scholar
  96. J. W. Pollard, “Trophic macrophages in development and disease,” Nature Reviews Immunology, vol. 9, no. 4, pp. 259–270, 2009. View at Publisher · View at Google Scholar · View at Scopus
  97. C. Steidl, T. Lee, S. P. Shah et al., “Tumor-associated macrophages and survival in classic Hodgkin's lymphoma,” The New England Journal of Medicine, vol. 362, no. 10, pp. 875–885, 2010. View at Publisher · View at Google Scholar · View at Scopus
  98. C. Subimerb, S. Pinlaor, N. Khuntikeo et al., “Tissue invasive macrophage density is correlated with prognosis in cholangiocarcinoma,” Molecular Medicine Reports, vol. 3, no. 4, pp. 597–605, 2010. View at Publisher · View at Google Scholar · View at Scopus
  99. H. Kurahara, S. Takao, K. Maemura et al., “M2-polarized tumor-associated macrophage infiltration of regional lymph nodes is associated with nodal lymphangiogenesis and occult nodal involvement in pN0 pancreatic cancer,” Pancreas, vol. 42, no. 1, pp. 155–159, 2013. View at Publisher · View at Google Scholar
  100. S. M. Mahmoud, A. H. Lee, E. C. Paish, R. D. Macmillan, I. O. Ellis, and A. R. Green, “Tumour-infiltrating macrophages and clinical outcome in breast cancer,” Journal of Clinical Pathology, vol. 65, no. 2, pp. 159–163, 2012. View at Publisher · View at Google Scholar
  101. Q. Wei, W. Fang, L. Ye et al., “Density of tumor-associated macrophages correlates with lymph node metastasis in papillary thyroid carcinoma,” Thyroid, vol. 22, no. 9, pp. 905–910, 2012. View at Google Scholar
  102. B. Z. Qian and J. W. Pollard, “Macrophage diversity enhances tumor progression and metastasis,” Cell, vol. 141, no. 1, pp. 39–51, 2010. View at Publisher · View at Google Scholar · View at Scopus
  103. A. Morandi, V. Barbetti, M. Riverso, P. Dello Sbarba, and E. Rovida, “The colony-stimulating factor-1 (CSF-1) receptor sustains ERK1/2 activation and proliferation in breast cancer cell lines,” PloS One, vol. 6, no. 11, Article ID e27450, 2011. View at Publisher · View at Google Scholar
  104. Y. Lee, M. Chittezhath, V. Andre et al., “Protumoral role of monocytes in human B-cell precursor acute lymphoblastic leukemia: involvement of the chemokine CXCL10,” Blood, vol. 119, no. 1, pp. 227–237, 2012. View at Publisher · View at Google Scholar
  105. N. B. Hao, M. H. Lu, Y. H. Fan, Y. L. Cao, Z. R. Zhang, and S. M. Yang, “Macrophages in tumor microenvironments and the progression of tumors,” Clinical & Developmental Immunology, vol. 2012, Article ID 948098, 11 pages, 2012. View at Publisher · View at Google Scholar
  106. P. D. Smith, L. E. Smythies, R. Shen, T. Greenwell-Wild, M. Gliozzi, and S. M. Wahl, “Intestinal macrophages and response to microbial encroachment,” Mucosal Immunology, vol. 4, no. 1, pp. 31–42, 2011. View at Publisher · View at Google Scholar · View at Scopus
  107. S. B. Weisser, H. K. Brugger, N. S. Voglmaier, K. W. McLarren, N. van Rooijen, and L. M. Sly, “SHIP-deficient, alternatively activated macrophages protect mice during DSS-induced colitis,” Journal of Leukocyte Biology, vol. 90, no. 3, pp. 483–492, 2011. View at Publisher · View at Google Scholar
  108. S. M. Wahl and W. Chen, “Transforming growth factor β-induced regulatory T cells referee inflammatory and autoimmune diseases,” Arthritis Research and Therapy, vol. 7, no. 2, pp. 62–68, 2005. View at Publisher · View at Google Scholar · View at Scopus
  109. P. Pandiyan, L. Zheng, S. Ishihara, J. Reed, and M. J. Lenardo, “CD4+CD25+Foxp3+ regulatory T cells induce cytokine deprivation-mediated apoptosis of effector CD4+ T cells,” Nature Immunology, vol. 8, no. 12, pp. 1353–1362, 2007. View at Publisher · View at Google Scholar · View at Scopus
  110. F. Baratelli, Y. Lin, L. Zhu et al., “Prostaglandin E2 induces FOXP3 gene expression and T regulatory cell function in human CD4+ T cells,” Journal of Immunology, vol. 175, no. 3, pp. 1483–1490, 2005. View at Google Scholar · View at Scopus
  111. J. Condeelis and J. W. Pollard, “Macrophages: obligate partners for tumor cell migration, invasion, and metastasis,” Cell, vol. 124, no. 2, pp. 263–266, 2006. View at Publisher · View at Google Scholar · View at Scopus
  112. T. L. Rogers and I. Holen, “Tumour macrophages as potential targets of bisphosphonates,” Journal of Translational Medicine, vol. 9, article 177, 2011. View at Publisher · View at Google Scholar
  113. A. Bellocq, M. Antoine, A. Flahault et al., “Neutrophil alveolitis in bronchioloalveolar carcinoma: induction by tumor-derived interleukin-8 and relation to clinical outcome,” American Journal of Pathology, vol. 152, no. 1, pp. 83–92, 1998. View at Google Scholar · View at Scopus
  114. L. A. Pekarek, B. A. Starr, A. Y. Toledano, and H. Schreiber, “Inhibition of tumor growth by elimination of granulocytes,” The Journal of Experimental Medicine, vol. 181, no. 1, pp. 435–440, 1995. View at Publisher · View at Google Scholar · View at Scopus
  115. H. K. Jensen, F. Donskov, N. Marcussen, M. Nordsmark, F. Lundbeck, and H. von der Maase, “Presence of intratumoral neutrophils is an independent prognostic factor in localized renal cell carcinoma,” Journal of Clinical Oncology, vol. 27, no. 28, pp. 4709–4717, 2009. View at Publisher · View at Google Scholar · View at Scopus
  116. M. Wislez, N. Rabbe, J. Marchal et al., “Hepatocyte growth factor production by neutrophils infiltrating bronchioloalveolar subtype pulmonary adenocarcinoma: role in tumor progression and death,” Cancer Research, vol. 63, no. 6, pp. 1405–1412, 2003. View at Google Scholar · View at Scopus
  117. M. Kowanetz, X. Wu, J. Lee et al., “Granulocyte-colony stimulating factor promotes lung metastasis through mobilization of Ly6G+Ly6C+ granulocytes,” Proceedings of the National Academy of Sciences of the United States of America, vol. 107, no. 50, pp. 21248–21255, 2010. View at Publisher · View at Google Scholar · View at Scopus
  118. A. M. Houghton, D. M. Rzymkiewicz, H. Ji et al., “Neutrophil elastase-mediated degradation of IRS-1 accelerates lung tumor growth,” Nature Medicine, vol. 16, no. 2, pp. 219–223, 2010. View at Publisher · View at Google Scholar · View at Scopus
  119. P. Conti, M. L. Castellani, D. Kempuraj et al., “Role of mast cells in tumor growth,” Annals of Clinical and Laboratory Science, vol. 37, no. 4, pp. 315–322, 2007. View at Google Scholar · View at Scopus
  120. B. Huang, Z. Lei, G. M. Zhang et al., “SCF-mediated mast cell infiltration and activation exacerbate the inflammation and immunosuppression in tumor microenvironment,” Blood, vol. 112, no. 4, pp. 1269–1279, 2008. View at Publisher · View at Google Scholar · View at Scopus
  121. K. Norrby, “Mast cells and angiogenesis,” APMIS, vol. 110, no. 5, pp. 355–371, 2002. View at Publisher · View at Google Scholar · View at Scopus
  122. L. M. Coussens, W. W. Raymond, G. Bergers et al., “Inflammatory mast cells up-regulate angiogenesis during squamous epithelial carcinogenesis,” Genes and Development, vol. 13, no. 11, pp. 1382–1397, 1999. View at Google Scholar · View at Scopus
  123. D. Ribatti and E. Crivellato, “The controversial role of mast cells in tumor growth,” International Review of Cell and Molecular Biology, vol. 275, pp. 89–131, 2009. View at Publisher · View at Google Scholar · View at Scopus
  124. A. Wasiuk, V. C. de Vries, K. Hartmann, A. Roers, and R. J. Noelle, “Mast cells as regulators of adaptive immunity to tumours,” Clinical and Experimental Immunology, vol. 155, no. 2, pp. 140–146, 2009. View at Publisher · View at Google Scholar · View at Scopus
  125. A. Mancino, T. Schioppa, P. Larghi et al., “Divergent effects of hypoxia on dendritic cell functions,” Blood, vol. 112, no. 9, pp. 3723–3734, 2008. View at Publisher · View at Google Scholar · View at Scopus
  126. A. R. Elia, P. Cappello, M. Puppo et al., “Human dendritic cells differentiated in hypoxia down-modulate antigen uptake and change their chemokine expression profile,” Journal of Leukocyte Biology, vol. 84, no. 6, pp. 1472–1482, 2008. View at Publisher · View at Google Scholar · View at Scopus
  127. M. Yang, C. Ma, S. Liu et al., “HIF-dependent induction of adenosine receptor A2b skews human dendritic cells to a Th2-stimulating phenotype under hypoxia,” Immunology and Cell Biology, vol. 88, no. 2, pp. 165–171, 2010. View at Publisher · View at Google Scholar · View at Scopus
  128. U. K. Scarlett, M. R. Rutkowski, A. M. Rauwerdink et al., “Ovarian cancer progression is controlled by phenotypic changes in dendritic cells,” The Journal of Experimental Medicine, vol. 209, no. 3, pp. 495–506, 2012. View at Publisher · View at Google Scholar
  129. S. V. Novitskiy, S. Ryzhov, R. Zaynagetdinov et al., “Adenosine receptors in regulation of dendritic cell differentiation and function,” Blood, vol. 112, no. 5, pp. 1822–1831, 2008. View at Publisher · View at Google Scholar · View at Scopus
  130. T. T. Tan and L. M. Coussens, “Humoral immunity, inflammation and cancer,” Current Opinion in Immunology, vol. 19, no. 2, pp. 209–216, 2007. View at Publisher · View at Google Scholar · View at Scopus
  131. D. G. DeNardo and L. M. Coussens, “Inflammation and breast cancer. Balancing immune response: crosstalk between adaptive and innate immune cells during breast cancer progression,” Breast Cancer Research, vol. 9, no. 4, p. 212, 2007. View at Google Scholar · View at Scopus
  132. J. M. Zapata, D. Llobet, M. Krajewska, S. Lefebvre, C. L. Kress, and J. C. Reed, “Lymphocyte-specific TRAF3 transgenic mice have enhanced humoral responses and develop plasmacytosis, autoimmunity, inflammation, and cancer,” Blood, vol. 113, no. 19, pp. 4595–4603, 2009. View at Publisher · View at Google Scholar · View at Scopus
  133. K. E. de Visser, L. V. Korets, and L. M. Coussens, “De novo carcinogenesis promoted by chronic inflammation is B lymphocyte dependent,” Cancer Cell, vol. 7, no. 5, pp. 411–423, 2005. View at Publisher · View at Google Scholar · View at Scopus
  134. J. E. Talmadge, M. Donkor, and E. Scholar, “Inflammatory cell infiltration of tumors: Jekyll or Hyde,” Cancer and Metastasis Reviews, vol. 26, no. 3-4, pp. 373–400, 2007. View at Publisher · View at Google Scholar · View at Scopus
  135. R. D. Schreiber, L. J. Old, and M. J. Smyth, “Cancer immunoediting: integrating immunity's roles in cancer suppression and promotion,” Science, vol. 331, no. 6024, pp. 1565–1570, 2011. View at Publisher · View at Google Scholar · View at Scopus
  136. M. D. Vesely, M. H. Kershaw, R. D. Schreiber, and M. J. Smyth, “Natural innate and adaptive immunity to cancer,” Annual Review of Immunology, vol. 29, pp. 235–271, 2011. View at Publisher · View at Google Scholar · View at Scopus
  137. S. Z. Josefowicz, L. F. Lu, and A. Y. Rudensky, “Regulatory T cells: mechanisms of differentiation and function,” Annual Review of Immunology, vol. 30, pp. 531–564, 2012. View at Publisher · View at Google Scholar
  138. S. Onizuka, I. Tawara, J. Shimizu, S. Sakaguchi, T. Fujita, and E. Nakayama, “Tumor rejection by in vivo administration of anti-CD25 (interleukin-2 receptor α) monoclonal antibody,” Cancer Research, vol. 59, no. 13, pp. 3128–3133, 1999. View at Google Scholar · View at Scopus
  139. F. Driessler, K. Venstrom, R. Sabat, K. Asadullah, and A. J. Schottelius, “Molecular mechanisms of interleukin-10-mediated inhibition of NF-κB activity: a role for p50,” Clinical and Experimental Immunology, vol. 135, no. 1, pp. 64–73, 2004. View at Publisher · View at Google Scholar · View at Scopus
  140. W. Ouyang, S. Rutz, N. K. Crellin, P. A. Valdez, and S. G. Hymowitz, “Regulation and functions of the IL-10 family of cytokines in inflammation and disease,” Annual Review of Immunology, vol. 29, pp. 71–109, 2011. View at Publisher · View at Google Scholar · View at Scopus
  141. P. A. Prieto, J. C. Yang, R. M. Sherry et al., “CTLA-4 blockade with ipilimumab: long-term follow-up of 177 patients with metastatic melanoma,” Clinical Cancer Research, vol. 18, pp. 2039–2047, 2012. View at Publisher · View at Google Scholar
  142. G. Zhou and H. Levitsky, “Towards curative cancer immunotherapy: overcoming posttherapy tumor escape,” Clinical and Developmental Immunology, vol. 2012, Article ID 124187, 12 pages, 2012. View at Publisher · View at Google Scholar
  143. D. I. Gabrilovich and S. Nagaraj, “Myeloid-derived suppressor cells as regulators of the immune system,” Nature Reviews Immunology, vol. 9, no. 3, pp. 162–174, 2009. View at Publisher · View at Google Scholar · View at Scopus
  144. A. S. Pak, M. A. Wright, J. P. Matthews, S. L. Collins, G. J. Petruzzelli, and M. R. I. Young, “Mechanisms of immune suppression in patients with head and neck cancer: presence of CD34+ cells which suppress immune functions within cancers that secrete granulocyte-macrophage colony-stimulating factor,” Clinical Cancer Research, vol. 1, no. 1, pp. 95–103, 1995. View at Google Scholar · View at Scopus
  145. M. R. I. Young, K. Kolesiak, M. A. Wright, and D. I. Gabrilovich, “Chemoattraction of femoral CD34+ progenitor cells by tumor-derived vascular endothelial cell growth factor,” Clinical and Experimental Metastasis, vol. 17, no. 10, pp. 881–888, 1999. View at Publisher · View at Google Scholar · View at Scopus
  146. M. R. I. Young and M. A. Wright, “Myelopoiesis-associated immune suppressor cells in mice bearing metastatic Lewis lung carcinoma tumors: γ interferon plus tumor necrosis factor α synergistically reduces immune suppressor and tumor growth-promoting activities of bone marrow cells and diminishes tumor recurrence and metastasis,” Cancer Research, vol. 52, no. 22, pp. 6335–6340, 1992. View at Google Scholar · View at Scopus
  147. E. Peranzoni, S. Zilio, I. Marigo et al., “Myeloid-derived suppressor cell heterogeneity and subset definition,” Current Opinion in Immunology, vol. 22, no. 2, pp. 238–244, 2010. View at Publisher · View at Google Scholar · View at Scopus
  148. T. F. Greten, M. P. Manns, and F. Korangy, “Myeloid derived suppressor cells in human diseases,” International Immunopharmacology, vol. 11, no. 7, pp. 802–806, 2011. View at Publisher · View at Google Scholar · View at Scopus
  149. P. Filipazzi, R. Valenti, V. Huber et al., “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,” Journal of Clinical Oncology, vol. 25, no. 18, pp. 2546–2553, 2007. View at Publisher · View at Google Scholar · View at Scopus
  150. J. D. Waight, Q. Hu, A. Miller, S. Liu, and S. I. Abrams, “Tumor-derived G-CSF facilitates neoplastic growth through a granulocytic myeloid-derived suppressor cell-dependent mechanism,” PloS One, vol. 6, Article ID e27690, 2011. View at Google Scholar
  151. D. B. Stairs, L. J. Bayne, B. Rhoades et al., “Deletion of p120-catenin results in a tumor microenvironment with inflammation and cancer that establishes it as a tumor suppressor gene,” Cancer Cell, vol. 19, no. 4, pp. 470–483, 2011. View at Publisher · View at Google Scholar · View at Scopus
  152. N. Dilek, R. Vuillefroy de Silly, G. Blancho, and B. Vanhove, “Myeloid-derived suppressor cells: mechanisms of action and recent advances in their role in transplant tolerance,” Frontiers in Immunology, vol. 3, p. 208, 2012. View at Publisher · View at Google Scholar
  153. S. Nagaraj and D. I. Gabrilovich, “Tumor escape mechanism governed by myeloid-derived suppressor cells,” Cancer Research, vol. 68, no. 8, pp. 2561–2563, 2008. View at Publisher · View at Google Scholar · View at Scopus
  154. S. Ostrand-Rosenberg and P. Sinha, “Myeloid-derived suppressor cells: linking inflammation and cancer,” Journal of Immunology, vol. 182, no. 8, pp. 4499–4506, 2009. View at Publisher · View at Google Scholar · View at Scopus
  155. A. Sica and V. Bronte, “Altered macrophage differentiation and immune dysfunction in tumor development,” Journal of Clinical Investigation, vol. 117, no. 5, pp. 1155–1166, 2007. View at Publisher · View at Google Scholar · View at Scopus
  156. E. M. Hanson, V. K. Clements, P. Sinha, D. Ilkovitch, and S. Ostrand-Rosenberg, “Myeloid-derived suppressor cells down-regulate L-selectin expression on CD4+ and CD8+ T cells,” Journal of Immunology, vol. 183, no. 2, pp. 937–944, 2009. View at Publisher · View at Google Scholar · View at Scopus
  157. B. Molon, S. Ugel, F. Del Pozzo et al., “Chemokine nitration prevents intratumoral infiltration of antigen-specific T cells,” The Journal of Experimental Medicine, vol. 208, no. 10, pp. 1949–1962, 2011. View at Publisher · View at Google Scholar
  158. P. Y. Pan, G. Ma, K. J. Weber et al., “Immune stimulatory receptor CD40 is required for T-cell suppression and T regulatory cell activation mediated by myeloid-derived suppressor cells in cancer,” Cancer Research, vol. 70, no. 1, pp. 99–108, 2010. View at Publisher · View at Google Scholar · View at Scopus
  159. B. Huang, P. Y. Pan, Q. Li et al., “Gr-1+CD115+ immature myeloid suppressor cells mediate the development of tumor-induced T regulatory cells and T-cell anergy in tumor-bearing host,” Cancer Research, vol. 66, no. 2, pp. 1123–1131, 2006. View at Publisher · View at Google Scholar · View at Scopus
  160. S. M. Centuori, M. Trad, C. J. Lacasse et al., “Myeloid-derived suppressor cells from tumor-bearing mice impair TGF-β-induced differentiation of CD4+CD25+Foxp3+ Tregs from CD4+CD25FoxP3 T cells,” Journal of Leukocyte Biology, vol. 92, no. 5, pp. 987–997, 2012. View at Publisher · View at Google Scholar
  161. H. Li, Y. Han, Q. Guo, M. Zhang, and X. Cao, “Cancer-expanded myeloid-derived suppressor cells induce anergy of NK cells through membrane-bound TGF-β1,” Journal of Immunology, vol. 182, no. 1, pp. 240–249, 2009. View at Google Scholar · View at Scopus
  162. E. Suzuki, V. Kapoor, A. S. Jassar, L. R. Kaiser, and S. M. Albelda, “Gemcitabine selectively eliminates splenic Gr-1+/CD11b + myeloid suppressor cells in tumor-bearing animals and enhances antitumor immune activity,” Clinical Cancer Research, vol. 11, no. 18, pp. 6713–6721, 2005. View at Publisher · View at Google Scholar · View at Scopus
  163. Y. Narita, D. Wakita, T. Ohkuri, K. Chamoto, and T. Nishimura, “Potential differentiation of tumor bearing mouse CD11b+Gr-1+ immature myeloid cells into both suppressor macrophages and immunostimulatory dendritic cells,” Biomedical Research, vol. 30, no. 1, pp. 7–15, 2009. View at Google Scholar · View at Scopus
  164. C. A. Corzo, T. Condamine, L. Lu et al., “HIF-1α regulates function and differentiation of myeloid-derived suppressor cells in the tumor microenvironment,” The Journal of Experimental Medicine, vol. 207, no. 11, pp. 2439–2453, 2010. View at Publisher · View at Google Scholar · View at Scopus
  165. L. Yang, L. M. DeBusk, K. Fukuda et al., “Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis,” Cancer Cell, vol. 6, no. 4, pp. 409–421, 2004. View at Publisher · View at Google Scholar · View at Scopus
  166. B. Toh, X. Wang, J. Keeble et al., “Mesenchymal transition and dissemination of cancer cells is driven by myeloid-derived suppressor cells infiltrating the primary tumor,” PLoS Biology, vol. 9, Article ID e1001162, 2011. View at Google Scholar
  167. S. Grivennikov, E. Karin, J. Terzic et al., “IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer,” Cancer Cell, vol. 15, no. 2, pp. 103–113, 2009. View at Publisher · View at Google Scholar · View at Scopus
  168. M. Lesina, M. U. Kurkowski, K. Ludes et al., “Stat3/Socs3 activation by IL-6 transsignaling promotes progression of pancreatic intraepithelial neoplasia and development of pancreatic cancer,” Cancer Cell, vol. 19, no. 4, pp. 456–469, 2011. View at Publisher · View at Google Scholar · View at Scopus
  169. F. Abe, A. J. Dafferner, M. Donkor et al., “Myeloid-derived suppressor cells in mammary tumor progression in FVB Neu transgenic mice,” Cancer Immunology, Immunotherapy, vol. 59, no. 1, pp. 47–62, 2010. View at Publisher · View at Google Scholar · View at Scopus
  170. C. M. Diaz-Montero, M. L. Salem, M. I. Nishimura, E. Garrett-Mayer, D. J. Cole, and A. J. Montero, “Increased circulating myeloid-derived suppressor cells correlate with clinical cancer stage, metastatic tumor burden, and doxorubicin-cyclophosphamide chemotherapy,” Cancer Immunology, Immunotherapy, vol. 58, no. 1, pp. 49–59, 2009. View at Publisher · View at Google Scholar · View at Scopus
  171. S. Solito, E. Falisi, C. M. Diaz-Montero et al., “A human promyelocytic-like population is responsible for the immune suppression mediated by myeloid-derived suppressor cells,” Blood, vol. 118, pp. 2254–2265, 2011. View at Publisher · View at Google Scholar
  172. B. Raychaudhuri, P. Rayman, J. Ireland et al., “Myeloid-derived suppressor cell accumulation and function in patients with newly diagnosed glioblastoma,” Neuro-Oncology, vol. 13, no. 6, pp. 591–599, 2011. View at Publisher · View at Google Scholar · View at Scopus
  173. S. Ostrand-Rosenberg, P. Sinha, D. W. Beury, and V. K. Clements, “Cross-talk between myeloid-derived suppressor cells (MDSC), macrophages, and dendritic cells enhances tumor-induced immune suppression,” Seminars in Cancer Biology, vol. 22, no. 4, pp. 275–281, 2012. View at Publisher · View at Google Scholar
  174. J. C. Ochando and S. H. Chen, “Myeloid-derived suppressor cells in transplantation and cancer,” Immunologic Research, vol. 54, no. 1–3, pp. 275–285, 2012. View at Publisher · View at Google Scholar