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Journal of Immunology Research
Volume 2016, Article ID 9720912, 12 pages
http://dx.doi.org/10.1155/2016/9720912
Review Article

New Mechanisms of Tumor-Associated Macrophages on Promoting Tumor Progression: Recent Research Advances and Potential Targets for Tumor Immunotherapy

1Department of Oncology, Guang’anmen Hospital, China Academy of Chinese Medicine Sciences, No. 5 Beixiange, Xicheng District, Beijing 100053, China
2Beijing University of Chinese Medicine, No. 11 North Third Ring Road East, Chaoyang District, Beijing 100029, China
3Department of Oncology, Xiyuan Hospital, China Academy of Chinese Medicine Sciences, No. 1 Playground Road, Haidian District, Beijing 100091, China
4Institute of Basic Research in Clinical Medicine (IBRCM), China Academy of Chinese Medicine Sciences, No. 16 Dongzhimen Nanxiaojie, Dongcheng District, Beijing 100700, China

Received 20 June 2016; Accepted 26 September 2016

Academic Editor: Eyad Elkord

Copyright © 2016 Qiujun Guo 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. V. Gocheva, H.-W. Wang, B. B. Gadea et al., “IL-4 induces cathepsin protease activity in tumor-associated macrophages to promote cancer growth and invasion,” Genes and Development, vol. 24, no. 3, pp. 241–255, 2010. View at Publisher · View at Google Scholar · View at Scopus
  2. A. Sica, T. Schioppa, A. Mantovani, and P. Allavena, “Tumour-associated macrophages are a distinct M2 polarised population promoting tumour progression: potential targets of anti-cancer therapy,” European Journal of Cancer, vol. 42, no. 6, pp. 717–727, 2006. View at Publisher · View at Google Scholar · View at Scopus
  3. R. Wang, J. Zhang, S. Chen et al., “Tumor-associated macrophages provide a suitable microenvironment for non-small lung cancer invasion and progression,” Lung Cancer, vol. 74, no. 2, pp. 188–196, 2011. View at Publisher · View at Google Scholar · View at Scopus
  4. S. Edin, M. L. Wikberg, P.-A. Oldenborg, and R. Palmqvist, “Macrophages: good guys in colorectal cancer,” OncoImmunology, vol. 2, no. 2, article e23038, 2013. View at Publisher · View at Google Scholar · View at Scopus
  5. T. K. Owonikoko, S. E. Dahlberg, S. A. Khan et al., “A phase 1 safety study of veliparib combined with cisplatin and etoposide in extensive stage small cell lung cancer: a trial of the ECOG-ACRIN Cancer Research Group (E2511),” Lung Cancer, vol. 89, no. 1, pp. 66–70, 2015. View at Publisher · View at Google Scholar · View at Scopus
  6. W. H. Wilson, “Treatment strategies for aggressive lymphomas: what works?” Hematology, vol. 2013, no. 1, pp. 584–590, 2013. View at Google Scholar · View at Scopus
  7. D. Li and E. M. O'Reilly, “Adjuvant and neoadjuvant systemic therapy for pancreas adenocarcinoma,” Seminars in Oncology, vol. 42, no. 1, pp. 134–143, 2015. View at Publisher · View at Google Scholar · View at Scopus
  8. K. Sugimura, H. Miyata, K. Tanaka et al., “High infiltration of tumor-associated macrophages is associated with a poor response to chemotherapy and poor prognosis of patients undergoing neoadjuvant chemotherapy for esophageal cancer,” Journal of Surgical Oncology, vol. 111, no. 6, pp. 752–759, 2015. View at Publisher · View at Google Scholar · View at Scopus
  9. B. X. Pei, B. S. Sun, Z. F. Zhang, A. L. Wang, and P. Ren, “Interstitial tumor-associated macrophages combined with tumor-derived colony-stimulating factor-1 and interleukin-6, a novel prognostic biomarker in non–small cell lung cancer,” Journal of Thoracic & Cardiovascular Surgery, vol. 148, no. 4, pp. 1208–1216, 2014. View at Google Scholar
  10. M. Amit and Z. Gil, “Macrophages increase the resistance of pancreatic adenocarcinoma cells to gemcitabine by upregulating cytidine deaminase,” OncoImmunology, vol. 2, no. 12, Article ID e27231, 2013. View at Publisher · View at Google Scholar · View at Scopus
  11. C. Yang, L. He, P. He et al., “Increased drug resistance in breast cancer by tumor-associated macrophages through IL-10/STAT3/bcl-2 signaling pathway,” Medical Oncology, vol. 32, no. 2, pp. 1–8, 2015. View at Publisher · View at Google Scholar · View at Scopus
  12. Q.-J. Xuan, J.-X. Wang, A. Nanding et al., “Tumor-associated macrophages are correlated with tamoxifen resistance in the postmenopausal breast cancer patients,” Pathology and Oncology Research, vol. 20, no. 3, pp. 619–624, 2014. View at Publisher · View at Google Scholar · View at Scopus
  13. F.-T. Chung, K.-Y. Lee, C.-W. Wang et al., “Tumor-associated macrophages correlate with response to epidermal growth factor receptor-tyrosine kinase inhibitors in advanced non-small cell lung cancer,” International Journal of Cancer, vol. 131, no. 3, pp. E227–E235, 2012. View at Publisher · View at Google Scholar · View at Scopus
  14. J. S. Russell and J. M. Brown, “The irradiated tumor microenvironment: role of tumor-associated macrophages in vascular recovery,” Frontiers in Physiology, vol. 4, article 157, 2013. View at Publisher · View at Google Scholar · View at Scopus
  15. M. Timaner, R. Bril, O. Kaidar-Person et al., “Dequalinium blocks macrophage-induced metastasis following local radiation,” Oncotarget, vol. 6, no. 29, pp. 27537–27554, 2015. View at Publisher · View at Google Scholar · View at Scopus
  16. T. A. Wynn, A. Chawla, and J. W. Pollard, “Macrophage biology in development, homeostasis and disease,” Nature, vol. 496, no. 7446, pp. 445–455, 2013. View at Publisher · View at Google Scholar · View at Scopus
  17. L. Milas, J. Wike, N. Hunter, J. Volpe, and I. Basic, “Macrophage content of murine sarcomas and carcinomas: associations with tumor growth parameters and tumor radiocurability,” Cancer Research, vol. 47, no. 4, pp. 1069–1075, 1987. View at Google Scholar · View at Scopus
  18. S. L. Shiao, B. Ruffell, D. G. DeNardo, B. A. Faddegon, C. C. Park, and L. M. Coussens, “TH2-polarized CD4+ T cells and macrophages limit efficacy of radiotherapy,” Cancer Immunology Research, vol. 3, no. 5, pp. 518–525, 2015. View at Publisher · View at Google Scholar
  19. C. Guo, A. Buranych, D. Sarkar, P. B. Fisher, and X. Y. Wang, “The role of tumor-associated macrophages in tumor vascularization,” Vasc Cell, vol. 15, no. 8, pp. 917–927, 2013. View at Google Scholar
  20. A. Teresa Pinto, M. Laranjeiro Pinto, A. Patrícia Cardoso et al., “Ionizing radiation modulates human macrophages towards a pro-inflammatory phenotype preserving their pro-invasive and pro-angiogenic capacities,” Scientific Reports, vol. 6, Article ID 18765, 2016. View at Publisher · View at Google Scholar · View at Scopus
  21. C. Dong, M. He, W. Tu et al., “The differential role of human macrophage in triggering secondary bystander effects after either gamma-ray or carbon beam irradiation,” Cancer Letters, vol. 363, no. 1, pp. 92–100, 2015. View at Publisher · View at Google Scholar · View at Scopus
  22. C.-S. Chiang, S. Y. Fu, S.-C. Wang et al., “Irradiation promotes an M2 macrophage phenotype in tumor hypoxia,” Frontiers in Oncology, vol. 2, article 89, 2012. View at Publisher · View at Google Scholar · View at Scopus
  23. J. Xu, J. Escamilla, S. Mok et al., “CSF1R signaling blockade stanches tumor-infiltrating myeloid cells and improves the efficacy of radiotherapy in prostate cancer,” Cancer Research, vol. 73, no. 9, pp. 2782–2794, 2013. View at Publisher · View at Google Scholar · View at Scopus
  24. E. I. Ager, S. V. Kozin, N. D. Kirkpatrick et al., “Blockade of MMP14 activity in murine breast carcinomas: implications for macrophages, vessels, and radiotherapy,” Journal of the National Cancer Institute, vol. 107, no. 4, 2015. View at Publisher · View at Google Scholar · View at Scopus
  25. J. M. Gwak, M. H. Jang, D. I. Kim, A. N. Seo, and S. Y. Park, “Prognostic value of tumor-associated macrophages according to histologic locations and hormone receptor status in breast cancer,” PLoS ONE, vol. 10, no. 4, Article ID e0125728, 2015. View at Publisher · View at Google Scholar · View at Scopus
  26. Z.-Y. Yuan, R.-Z. Luo, R.-J. Peng, S.-S. Wang, and C. Xue, “High infiltration of tumor-associated macrophages in triple-negative breast cancer is associated with a higher risk of distant metastasis,” OncoTargets and Therapy, vol. 7, pp. 1475–1480, 2014. View at Publisher · View at Google Scholar · View at Scopus
  27. C.-N. Lin, C.-J. Wang, Y.-J. Chao, M.-D. Lai, and Y.-S. Shan, “The significance of the co-existence of osteopontin and tumor-associated macrophages in gastric cancer progression,” BMC Cancer, vol. 15, no. 1, article 128, 2015. View at Publisher · View at Google Scholar · View at Scopus
  28. L. Yang, F. Wang, L. Wang et al., “CD163+ tumor-associated macrophage is a prognostic biomarker and is associated with therapeutic effect on malignant pleural effusion of lung cancer patients,” Oncotarget, vol. 6, no. 12, pp. 10592–10603, 2015. View at Publisher · View at Google Scholar · View at Scopus
  29. Y. Li, B.-S. Sun, B. Pei et al., “Osteopontin-expressing macrophages in non-small cell lung cancer predict survival,” Annals of Thoracic Surgery, vol. 99, no. 4, pp. 1140–1148, 2015. View at Publisher · View at Google Scholar · View at Scopus
  30. Y.-H. Ni, L. Ding, X.-F. Huang, Y.-C. Dong, Q.-G. Hu, and Y.-Y. Hou, “Microlocalization of CD68+ tumor-associated macrophages in tumor stroma correlated with poor clinical outcomes in oral squamous cell carcinoma patients,” Tumor Biology, vol. 36, no. 7, pp. 5291–5298, 2015. View at Publisher · View at Google Scholar · View at Scopus
  31. K.-F. He, L. Zhang, C.-F. Huang et al., “CD163+ tumor-associated macrophages correlated with poor prognosis and cancer stem cells in oral squamous cell carcinoma,” BioMed Research International, vol. 2014, Article ID 838632, 9 pages, 2014. View at Publisher · View at Google Scholar · View at Scopus
  32. S. Wang, M. Sun, C. Gu et al., “Expression of CD163, interleukin-10, and interferon-gamma in oral squamous cell carcinoma: mutual relationships and prognostic implications,” European Journal of Oral Sciences, vol. 122, no. 3, pp. 202–209, 2014. View at Publisher · View at Google Scholar · View at Scopus
  33. I. H. Wei, C. M. Harmon, M. Arcerito, D. F. Cheng, R. M. Minter, and D. M. Simeone, “Tumor-associated macrophages are a useful biomarker to predict recurrence after surgical resection of nonfunctional pancreatic neuroendocrine tumors,” Annals of Surgery, vol. 260, no. 6, pp. 1088–1094, 2014. View at Publisher · View at Google Scholar · View at Scopus
  34. P. Ding, W. Wang, J. Wang, Z. Yang, and L. Xue, “Expression of tumor-associated macrophage in progression of human glioma,” Cell Biochemistry and Biophysics, vol. 70, no. 3, pp. 1625–1631, 2014. View at Publisher · View at Google Scholar · View at Scopus
  35. M. Illemann, O. D. Laerum, J. P. Hasselby et al., “Urokinase-type plasminogen activator receptor (uPAR) on tumor-associated macrophages is a marker of poor prognosis in colorectal cancer,” Cancer Medicine, vol. 3, no. 4, pp. 855–864, 2014. View at Publisher · View at Google Scholar · View at Scopus
  36. M. Kinouchi, K. Miura, T. Mizoi et al., “Infiltration of CD40-positive tumor-associated macrophages indicates a favorable prognosis in colorectal cancer patients,” Hepato-Gastroenterology, vol. 60, no. 121, pp. 83–88, 2013. View at Publisher · View at Google Scholar · View at Scopus
  37. Y.-C. Hou, Y.-J. Chao, H.-L. Tung, H.-C. Wang, and Y.-S. Shan, “Coexpression of CD44-positive/CD133-positive cancer stem cells and CD204-positive tumor-associated macrophages is a predictor of survival in pancreatic ductal adenocarcinoma,” Cancer, vol. 120, no. 17, pp. 2766–2777, 2014. View at Publisher · View at Google Scholar · View at Scopus
  38. C. Lan, X. Huang, S. Lin et al., “Expression of M2-polarized macrophages is associated with poor prognosis for advanced epithelial ovarian cancer,” Technology in Cancer Research & Treatment, vol. 12, no. 3, pp. 259–267, 2013. View at Publisher · View at Google Scholar · View at Scopus
  39. H. Takayama, K. Nishimura, A. Tsujimura et al., “Increased infiltration of tumor associated macrophages is associated with poor prognosis of bladder carcinoma in situ after intravesical bacillus calmette-guerin instillation,” Journal of Urology, vol. 181, no. 4, pp. 1894–1900, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. X.-F. Jiang, Q.-L. Tang, X.-M. Shen et al., “Tumor-associated macrophages, epidermal growth factor receptor correlated with the triple negative phenotype in endometrial endometrioid adenocarcinoma,” Pathology Research and Practice, vol. 208, no. 12, pp. 730–735, 2012. View at Publisher · View at Google Scholar · View at Scopus
  41. K. Gollapudi, C. Galet, T. Grogan et al., “Association between tumor-associated macrophage infiltration, high grade prostate cancer, and biochemical recurrence after radical prostatectomy,” American Journal of Cancer Research, vol. 3, no. 5, pp. 523–529, 2013. View at Google Scholar
  42. W. Hu, Y. Qian, F. Yu et al., “Alternatively activated macrophages are associated with metastasis and poor prognosis in prostate adenocarcinoma,” Oncology Letters, vol. 10, no. 3, pp. 1390–1396, 2015. View at Publisher · View at Google Scholar · View at Scopus
  43. D. W. Scott and C. Steidl, “The classical Hodgkin lymphoma tumor microenvironment: macrophages and gene expression-based modeling,” Hematology, vol. 2014, no. 1, pp. 144–150, 2014. View at Publisher · View at Google Scholar · View at Scopus
  44. T. Sasayama, K. Tanaka, T. Mizowaki et al., “Tumor-associated macrophages associate with cerebrospinal fluid interleukin-10 and survival in Primary Central Nervous System Lymphoma (PCNSL),” Brain Pathology, vol. 26, no. 4, pp. 479–487, 2016. View at Publisher · View at Google Scholar · View at Scopus
  45. W. Zhang, L. Wang, D. Zhou, Q. Cui, D. Zhao, and Y. Wu, “Expression of tumor-associated macrophages and vascular endothelial growth factor correlates with poor prognosis of peripheral T-cell lymphoma, not otherwise specified,” Leukemia and Lymphoma, vol. 52, no. 1, pp. 46–52, 2011. View at Publisher · View at Google Scholar · View at Scopus
  46. Q.-C. Cai, H. Liao, S.-X. Lin et al., “High expression of tumor-infiltrating macrophages correlates with poor prognosis in patients with diffuse large B-cell lymphoma,” Medical Oncology, vol. 29, no. 4, pp. 2317–2322, 2012. View at Publisher · View at Google Scholar · View at Scopus
  47. Q. Guo, J. Li, and H. Lin, “Effect and molecular mechanisms of traditional Chinese medicine on regulating tumor immunosuppressive microenvironment,” BioMed Research International, vol. 2015, Article ID 261620, 12 pages, 2015. View at Publisher · View at Google Scholar · View at Scopus
  48. J. Kim and J.-S. Bae, “Tumor-associated macrophages and neutrophils in tumor microenvironment,” Mediators of Inflammation, vol. 2016, Article ID 6058147, 11 pages, 2016. View at Publisher · View at Google Scholar · View at Scopus
  49. N. L. Costa, M. C. Valadares, P. P. C. Souza et al., “Tumor-associated macrophages and the profile of inflammatory cytokines in oral squamous cell carcinoma,” Oral Oncology, vol. 49, no. 3, pp. 216–223, 2013. View at Publisher · View at Google Scholar · View at Scopus
  50. Q. Han, H. Shi, and F. Liu, “CD163+ M2-type tumor-associated macrophage support the suppression of tumor-infiltrating T cells in osteosarcoma,” International Immunopharmacology, vol. 34, pp. 101–106, 2016. View at Publisher · View at Google Scholar
  51. T. Krneta, A. Gillgrass, and A. A. Ashkar, “The influence of macrophages and the tumor microenvironment on natural killer cells,” Current Molecular Medicine, vol. 13, no. 1, pp. 68–79, 2013. View at Publisher · View at Google Scholar · View at Scopus
  52. Q.-J. Guo and J. Li, “The role of tumor-associated macrophages in remodeling tumor immune microenvironment,” Tumor, vol. 33, no. 10, pp. 922–927, 2013. View at Publisher · View at Google Scholar · View at Scopus
  53. M. C. Schmid and J. A. Varner, “Myeloid cells in tumor inflammation,” Vascular Cell, vol. 4, article no. 14, 2012. View at Publisher · View at Google Scholar · View at Scopus
  54. M. Lohela, A.-J. Casbon, A. Olow et al., “Intravital imaging reveals distinct responses of depleting dynamic tumor-associated macrophage and dendritic cell subpopulations,” Proceedings of the National Academy of Sciences of the United States of America, vol. 111, no. 47, pp. E5086–E5095, 2014. View at Publisher · View at Google Scholar · View at Scopus
  55. P. C. Rodriguez, D. G. Quiceno, J. Zabaleta et al., “Arginase I production in the tumor microenvironment by mature myeloid cells inhibits T-cell receptor expression and antigen-specific T-cell responses,” Cancer Research, vol. 64, no. 16, pp. 5839–5849, 2004. View at Publisher · View at Google Scholar · View at Scopus
  56. T. Lu, R. Ramakrishnan, S. Altiok et al., “Tumor-infiltrating myeloid cells induce tumor cell resistance to cytotoxic T cells in mice,” Journal of Clinical Investigation, vol. 121, no. 10, pp. 4015–4029, 2011. View at Publisher · View at Google Scholar · View at Scopus
  57. A. Kondo, T. Yamashita, H. Tamura et al., “Interferon-γ and tumor necrosis factor-α induce an immunoinhibitory molecule, B7-H1, via nuclear factor-κB activation in blasts in myelodysplastic syndromes,” Blood, vol. 116, no. 7, pp. 1124–1131, 2010. View at Publisher · View at Google Scholar · View at Scopus
  58. S. I. Grivennikov and M. Karin, “Inflammatory cytokines in cancer: tumour necrosis factor and interleukin 6 take the stage,” Annals of the Rheumatic Diseases, vol. 70, no. 1, pp. i104–i108, 2011. View at Publisher · View at Google Scholar · View at Scopus
  59. D. M. Mosser and J. P. Edwards, “Exploring the full spectrum of macrophage activation,” Nature Reviews Immunology, vol. 8, no. 12, pp. 958–969, 2008. View at Publisher · View at Google Scholar · View at Scopus
  60. F. Balkwill, K. A. Charles, and A. Mantovani, “Smoldering and polarized inflammation in the initiation and promotion of malignant disease,” Cancer Cell, vol. 7, no. 3, pp. 211–217, 2005. View at Publisher · View at Google Scholar · View at Scopus
  61. 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 · View at Scopus
  62. L. M. Coussens and Z. Werb, “Inflammation and cancer,” Nature, vol. 420, no. 6917, pp. 860–867, 2002. View at Publisher · View at Google Scholar · View at Scopus
  63. 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
  64. H. A. Smith and Y. Kang, “The metastasis-promoting roles of tumor-associated immune cells,” Journal of Molecular Medicine, vol. 91, no. 4, pp. 411–429, 2013. View at Publisher · View at Google Scholar · View at Scopus
  65. 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
  66. H. Wang, X. Wang, X. Li et al., “CD68+HLA-DR+ M1-like macrophages promote motility of HCC cells via NF-κB/FAK pathway,” Cancer Letters, vol. 345, no. 1, pp. 91–99, 2014. View at Publisher · View at Google Scholar · View at Scopus
  67. T. H. Xu, L. Wei, Y. Zhang et al., “Tumor-associated macrophage-derived IL-6 and IL-8 enhance invasive activity of LoVo cells induced by PRL-3 in a KCNN4 channel-dependent manner,” Bmc Cancer, vol. 14, no. 5, pp. 697–710, 2014. View at Publisher · View at Google Scholar
  68. B.-Z. Qian, J. Li, H. Zhang et al., “CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis,” Nature, vol. 475, no. 7355, pp. 222–225, 2011. View at Publisher · View at Google Scholar · View at Scopus
  69. T. Kitamura, B.-Z. Qian, D. Soong et al., “CCL2-induced chemokine cascade promotes breast cancer metastasis by enhancing retention of metastasis-associated macrophages,” Journal of Experimental Medicine, vol. 212, no. 7, pp. 1043–1059, 2015. View at Publisher · View at Google Scholar · View at Scopus
  70. Q. Chen, X. H.-F. Zhang, and J. Massagué, “Macrophage binding to receptor VCAM-1 transmits survival signals in breast cancer cells that invade the lungs,” Cancer Cell, vol. 20, no. 4, pp. 538–549, 2011. View at Publisher · View at Google Scholar · View at Scopus
  71. B. D. Robinson, G. L. Sica, Y.-F. Liu et al., “Tumor microenvironment of metastasis in human breast carcinoma: a potential prognostic marker linked to hematogenous dissemination,” Clinical Cancer Research, vol. 15, no. 7, pp. 2433–2441, 2009. View at Publisher · View at Google Scholar · View at Scopus
  72. J. P. Thiery, H. Acloque, R. Y. J. Huang, and M. A. Nieto, “Epithelial-mesenchymal transitions in development and disease,” Cell, vol. 139, no. 5, pp. 871–890, 2009. View at Publisher · View at Google Scholar · View at Scopus
  73. D. K. Gupta, N. Singh, and D. K. Sahu, “TGF-β mediated crosstalk between malignant hepatocyte and tumor microenvironment in hepatocellular carcinoma,” Cancer Growth & Metastasis, vol. 7, no. 7, pp. 1–8, 2014. View at Google Scholar
  74. M. De Palma and C. E. Lewis, “Macrophage regulation of tumor responses to anticancer therapies,” Cancer Cell, vol. 23, no. 3, pp. 277–286, 2013. View at Publisher · View at Google Scholar · View at Scopus
  75. C.-Y. Liu, J.-Y. Xu, X.-Y. Shi et al., “M2-polarized tumor-associated macrophages promoted epithelial-mesenchymal transition in pancreatic cancer cells, partially through TLR4/IL-10 signaling pathway,” Laboratory Investigation, vol. 93, no. 7, pp. 844–854, 2013. View at Publisher · View at Google Scholar · View at Scopus
  76. J. Ravi, M. Elbaz, N. A. Wani, M. W. Nasser, and R. K. Ganju, “Cannabinoid receptor-2 agonist inhibits macrophage induced EMT in non-small cell lung cancer by downregulation of EGFR pathway,” Molecular Carcinogenesis, 2016. View at Publisher · View at Google Scholar · View at Scopus
  77. L. Lin, Y.-S. Chen, Y.-D. Yao et al., “CCL18 from tumor-associated macrophages promotes angio-genesis in breast cancer,” Oncotarget, vol. 6, no. 33, pp. 34758–34773, 2015. View at Publisher · View at Google Scholar · View at Scopus
  78. B. R. Zetter, “Angiogenesis and tumor metastasis,” Annual Review of Medicine, vol. 49, no. 7170, pp. 407–424, 1998. View at Publisher · View at Google Scholar · View at Scopus
  79. X. Xia, R. Du, L. Zhao, W. Sun, and X. Wang, “Expression of AEG-1 and microvessel density correlates with metastasis and prognosis of oral squamous cell carcinoma,” Human Pathology, vol. 45, no. 4, pp. 858–865, 2014. View at Publisher · View at Google Scholar · View at Scopus
  80. S. Karaman and M. Detmar, “Mechanisms of lymphatic metastasis,” The Journal of Clinical Investigation, vol. 124, no. 3, pp. 922–928, 2014. View at Publisher · View at Google Scholar · View at Scopus
  81. S. A. Stacker, S. P. Williams, T. Karnezis, R. Shayan, S. B. Fox, and M. G. Achen, “Lymphangiogenesis and lymphatic vessel remodelling in cancer,” Nature Reviews Cancer, vol. 14, no. 3, pp. 159–172, 2014. View at Publisher · View at Google Scholar · View at Scopus
  82. Y. Yang, M. Sun, L. Wang, and B. Jiao, “HIFs, angiogenesis, and cancer,” Journal of Cellular Biochemistry, vol. 114, no. 5, pp. 967–974, 2013. View at Publisher · View at Google Scholar · View at Scopus
  83. J. M. Breuss and P. Uhrin, “VEGF-initiated angiogenesis and the uPA/uPAR system,” Cell Adhesion and Migration, vol. 6, no. 6, pp. 535–540, 2012. View at Publisher · View at Google Scholar · View at Scopus
  84. D. P. Toomey, J. F. Murphy, and K. C. Conlon, “COX-2, VEGF and tumour angiogenesis,” Surgeon Journal of the Royal Colleges of Surgeons of Edinburgh & Ireland, vol. 7, no. 7, pp. 174–180, 2009. View at Google Scholar
  85. I. F. Dunn, O. Heese, and P. M. Black, “Growth factors in glioma angiogenesis: FGFs, PDGF, EGF, and TGFs,” Journal of Neuro-Oncology, vol. 50, no. 1-2, pp. 121–137, 2000. View at Publisher · View at Google Scholar · View at Scopus
  86. E. Fagiani and G. Christofori, “Angiopoietins in angiogenesis,” Cancer Letters, vol. 328, no. 1, pp. 18–26, 2013. View at Publisher · View at Google Scholar · View at Scopus
  87. E.-J. Yeo, L. Cassetta, B.-Z. Qian et al., “Myeloid wnt7b mediates the angiogenic switch and metastasis in breast cancer,” Cancer Research, vol. 74, no. 11, pp. 2962–2973, 2014. View at Publisher · View at Google Scholar · View at Scopus
  88. E. I. Deryugina, E. Zajac, A. Juncker-Jensen, T. A. Kupriyanova, L. Welter, and J. P. Quigley, “Tissue-infiltrating neutrophils constitute the major in vivo source of angiogenesis-inducing MMP-9 in the tumor microenvironment,” Neoplasia, vol. 16, no. 10, pp. 771–788, 2014. View at Publisher · View at Google Scholar · View at Scopus
  89. G. Bergers and L. E. Benjamin, “Tumorigenesis and the angiogenic switch,” Nature Reviews Cancer, vol. 3, no. 6, pp. 401–410, 2003. View at Publisher · View at Google Scholar · View at Scopus
  90. E. I. Deryugina and J. P. Quigley, “Pleiotropic roles of matrix metalloproteinases in tumor angiogenesis: contrasting, overlapping and compensatory functions,” Biochimica et Biophysica Acta—Molecular Cell Research, vol. 1803, no. 1, pp. 103–120, 2010. View at Publisher · View at Google Scholar · View at Scopus
  91. A. Casazza, D. Laoui, M. Wenes et al., “Impeding macrophage entry into hypoxic tumor areas by Sema3A/Nrp1 signaling blockade inhibits angiogenesis and restores antitumor immunity,” Cancer Cell, vol. 24, no. 6, pp. 695–709, 2013. View at Publisher · View at Google Scholar · View at Scopus
  92. L. J. Mu, J. S. Wang, Y. Z. Chen et al., “Hypoxia-inducible factor-1α and semaphorin4d genes involved with tumor-associated macrophage-induced metastatic behavior and clinical significance in colon cancer,” Chinese Medical Journal, vol. 127, no. 20, pp. 3568–3575, 2014. View at Publisher · View at Google Scholar · View at Scopus
  93. D. Laoui, E. Van Overmeire, G. Di Conza et al., “Tumor hypoxia does not drive differentiation of tumor-associated macrophages but rather fine-tunes the M2-like macrophage population,” Cancer Research, vol. 74, no. 1, pp. 24–30, 2014. View at Google Scholar
  94. L. D. E. Jensen, R. Cao, E.-M. Hedlund et al., “Nitric oxide permits hypoxia-induced lymphatic perfusion by controlling arterial-lymphatic conduits in zebrafish and glass catfish,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 43, pp. 18408–18413, 2009. View at Publisher · View at Google Scholar · View at Scopus
  95. S. Liao and T. P. Padera, “Lymphatic function and immune regulation in health and disease,” Lymphatic Research and Biology, vol. 11, no. 3, pp. 136–143, 2013. View at Publisher · View at Google Scholar · View at Scopus
  96. S. G. Rockson, “Lymphatics: where the circulation meets the immune system,” Lymphatic Research & Biology, vol. 11, no. 3, p. 115, 2013. View at Publisher · View at Google Scholar · View at Scopus
  97. J. Wang, Y. Guo, B. Wang et al., “Lymphatic microvessel density and vascular endothelial growth factor-C and -D as prognostic factors in breast cancer: a systematic review and meta-analysis of the literature,” Molecular Biology Reports, vol. 39, no. 12, pp. 11153–11165, 2012. View at Publisher · View at Google Scholar · View at Scopus
  98. Y. Chen, J. Yan, Z. Wang et al., “A meta-analysis of the relationship between lymphatic microvessel density and the survival of patient with colorectal cancer,” Lymphology, vol. 46, no. 1, pp. 42–51, 2013. View at Google Scholar · View at Scopus
  99. I. Pastushenko, P. B. Vermeulen, F. J. Carapeto et al., “Blood microvessel density, lymphatic microvessel density and lymphatic invasion in predicting melanoma metastases: systematic review and meta-analysis,” British Journal of Dermatology, vol. 170, no. 1, pp. 66–77, 2014. View at Publisher · View at Google Scholar · View at Scopus
  100. J. Wang, K. Li, B. Wang, and J. Bi, “Lymphatic microvessel density as a prognostic factor in non-small cell lung carcinoma: a meta-analysis of the literature,” Molecular Biology Reports, vol. 39, no. 5, pp. 5331–5338, 2012. View at Publisher · View at Google Scholar · View at Scopus
  101. S. F. Schoppmann, A. Fenzl, K. Nagy et al., “VEGF-C expressing tumor-associated macrophages in lymph node positive breast cancer: impact on lymphangiogenesis and survival,” Surgery, vol. 139, no. 6, pp. 839–846, 2006. View at Publisher · View at Google Scholar · View at Scopus
  102. B. Zhang, G. Yao, Y. Zhang et al., “M2-Polarized tumor-associated macrophages are associated with poor prognoses resulting from accelerated lymphangiogenesis in lung adenocarcinoma,” Clinics, vol. 66, no. 11, pp. 1879–1886, 2011. View at Publisher · View at Google Scholar · View at Scopus
  103. S. F. Schoppmann, P. Birner, J. Stöckl et al., “Tumor-associated macrophages express lymphatic endothelial growth factors and are related to peritumoral lymphangiogenesis,” The American Journal of Pathology, vol. 161, no. 3, pp. 947–956, 2002. View at Publisher · View at Google Scholar · View at Scopus
  104. Z. Špirić, Ž. Eri, and M. Erić, “Significance of vascular endothelial growth factor (VEGF)-C and VEGF-D in the progression of cutaneous melanoma,” International Journal of Surgical Pathology, vol. 23, no. 8, pp. 629–637, 2015. View at Publisher · View at Google Scholar · View at Scopus
  105. 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 · View at Scopus
  106. Y.-F. Sun, Y. Xu, X.-R. Yang et al., “Circulating stem cell-like epithelial cell adhesion molecule-positive tumor cells indicate poor prognosis of hepatocellular carcinoma after curative resection,” Hepatology, vol. 57, no. 4, pp. 1458–1468, 2013. View at Publisher · View at Google Scholar · View at Scopus
  107. Z. Zhen, J. Ren, and M. O'Neil, “Impact of stem cell marker expression on recurrence of TACE-treated hepatocellular carcinoma post liver transplantation,” Bmc Cancer, vol. 12, no. 1, pp. 2604–2615, 2012. View at Google Scholar
  108. M. Jinushi, S. Chiba, H. Yoshiyama et al., “Tumor-associated macrophages regulate tumorigenicity and anticancer drug responses of cancer stem/initiating cells,” Proceedings of the National Academy of Sciences of the United States of America, vol. 108, no. 30, pp. 12425–12430, 2011. View at Publisher · View at Google Scholar · View at Scopus
  109. S. Schwitalla, A. A. Fingerle, P. Cammareri et al., “Intestinal tumorigenesis initiated by dedifferentiation and acquisition of stem-cell-like properties,” Cell, vol. 152, no. 1-2, pp. 25–38, 2013. View at Publisher · View at Google Scholar · View at Scopus
  110. J. Yang, D. Liao, C. Chen et al., “Tumor-associated macrophages regulate murine breast cancer stem cells through a novel paracrine egfr/stat3/sox-2 signaling pathway,” Stem Cells, vol. 31, no. 2, pp. 248–258, 2013. View at Publisher · View at Google Scholar · View at Scopus
  111. C. Zhang, X. Hu, X. Y. Liu et al., “Effect of tumor-associated macrophages on gastric cancer stem cell in omental milky spots and lymph node micrometastasis,” International Journal of Clinical & Experimental Pathology, vol. 8, no. 11, 2015. View at Google Scholar
  112. Q.-M. Fan, Y.-Y. Jing, G.-F. Yu et al., “Tumor-associated macrophages promote cancer stem cell-like properties via transforming growth factor-beta1-induced epithelial-mesenchymal transition in hepatocellular carcinoma,” Cancer Letters, vol. 352, no. 2, pp. 160–168, 2014. View at Publisher · View at Google Scholar · View at Scopus
  113. X.-Z. Ye, S.-L. Xu, Y.-H. Xin et al., “Tumor-associated microglia/macrophages enhance the invasion of glioma stem-like cells via TGF-β1 signaling pathway,” Journal of Immunology, vol. 189, no. 1, pp. 444–453, 2012. View at Publisher · View at Google Scholar · View at Scopus
  114. H. Lu, K. R. Clauser, W. L. Tam et al., “A breast cancer stem cell niche supported by juxtacrine signalling from monocytes and macrophages,” Nature Cell Biology, vol. 16, no. 11, pp. 1105–1117, 2014. View at Publisher · View at Google Scholar · View at Scopus
  115. X. Deng, P. Zhang, T. Liang, S. Deng, X. Chen, and L. Zhu, “Ovarian cancer stem cells induce the M2 polarization of macrophages through the PPARγ and NF-κB pathways,” International Journal of Molecular Medicine, vol. 36, no. 2, pp. 449–454, 2015. View at Publisher · View at Google Scholar · View at Scopus
  116. M. Jinushi, “Role of cancer stem cell-associated inflammation in creating pro-inflammatory tumorigenic microenvironments,” OncoImmunology, vol. 3, no. 5, Article ID e28862, 2014. View at Publisher · View at Google Scholar · View at Scopus
  117. T. Chen, X. Wang, L. Guo et al., “Embryonic stem cells promoting macrophage survival and function are crucial for teratoma development,” Frontiers in Immunology, vol. 5, article 275, 2014. View at Publisher · View at Google Scholar · View at Scopus
  118. C. D. Mills, L. L. Lenz, and R. A. Harris, “A breakthrough: macrophage-directed cancer immunotherapy,” Cancer Research, vol. 76, no. 3, pp. 513–516, 2016. View at Publisher · View at Google Scholar · View at Scopus
  119. C. Zhang, L. Gao, Y. Cai et al., “Inhibition of tumor growth and metastasis by photoimmunotherapy targeting tumor-associated macrophage in a sorafenib-resistant tumor model,” Innovation & Social Process, vol. 84, no. 9, pp. 127–136, 2016. View at Google Scholar
  120. S. Vinogradov, G. Warren, and X. Wei, “Macrophages associated with tumors as potential targets and therapeutic intermediates,” Nanomedicine, vol. 9, no. 5, pp. 695–707, 2014. View at Publisher · View at Google Scholar · View at Scopus
  121. D. Laoui, E. Van Overmeire, P. De Baetselier, J. A. Van Ginderachter, and G. Raes, “Functional relationship between tumor-associated macrophages and macrophage colony-stimulating factor as contributors to cancer progression,” Frontiers in Immunology, vol. 5, no. 5, article 489, 2014. View at Publisher · View at Google Scholar · View at Scopus
  122. V. Chitu and E. R. Stanley, “Colony-stimulating factor-1 in immunity and inflammation,” Current Opinion in Immunology, vol. 18, no. 1, pp. 39–48, 2006. View at Publisher · View at Google Scholar · View at Scopus
  123. S. M. Pyonteck, L. Akkari, A. J. Schuhmacher et al., “CSF-1R inhibition alters macrophage polarization and blocks glioma progression,” Nature Medicine, vol. 19, no. 10, pp. 1264–1272, 2013. View at Publisher · View at Google Scholar · View at Scopus
  124. C. H. Ries, M. A. Cannarile, S. Hoves et al., “Targeting tumor-associated macrophages with anti-CSF-1R antibody reveals a strategy for cancer therapy,” Cancer Cell, vol. 25, no. 6, pp. 846–859, 2014. View at Publisher · View at Google Scholar · View at Scopus
  125. F. Roth, A. C. De La Fuente, J. L. Vella, A. Zoso, L. Inverardi, and P. Serafini, “Aptamer-mediated blockade of IL4Rα triggers apoptosis of MDSCs and limits tumor progression,” Cancer Research, vol. 72, no. 6, pp. 1373–1383, 2012. View at Publisher · View at Google Scholar · View at Scopus
  126. P. Allavena, G. Germano, C. Belgiovine, M. D'Incalci, and A. Mantovani, “A drug from the sea that strikes tumor-associated macrophages,” OncoImmunology, vol. 2, no. 6, article e24614, 2013. View at Publisher · View at Google Scholar · View at Scopus
  127. G. Germano, R. Frapolli, C. Belgiovine et al., “Role of macrophage targeting in the antitumor activity of trabectedin,” Cancer Cell, vol. 23, no. 2, pp. 249–262, 2013. View at Publisher · View at Google Scholar · View at Scopus
  128. L. Leanza, M. Zoratti, E. Gulbins, and I. Szabò, “Induction of apoptosis in macrophages via Kv1.3 and Kv1.5 potassium channels,” Current Medicinal Chemistry, vol. 19, no. 31, pp. 5394–5404, 2012. View at Publisher · View at Google Scholar · View at Scopus
  129. R. A. Franklin and M. O. Li, “Ontogeny of tumor-associated macrophages and its implication in cancer regulation,” Trends in Cancer, vol. 2, no. 1, pp. 20–34, 2016. View at Publisher · View at Google Scholar
  130. S. Tao, Y. Ye, L. Xiaoguang et al., “Inhibition of tumor angiogenesis by interferon-γ by suppression of tumor-associated macrophage differentiation,” Oncology Research Featuring Preclinical & Clinical Cancer Therapeutics, vol. 21, no. 5, pp. 227–235, 2014. View at Google Scholar
  131. A. Mantovani, S. Sozzani, M. Locati, P. Allavena, and A. Sica, “Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes,” Trends in Immunology, vol. 23, no. 11, pp. 549–555, 2002. View at Publisher · View at Google Scholar · View at Scopus
  132. T. Chanmee, P. Ontong, K. Konno, and N. Itano, “Tumor-associated macrophages as major players in the tumor microenvironment,” Cancers, vol. 6, no. 3, pp. 1670–1690, 2014. View at Publisher · View at Google Scholar · View at Scopus
  133. R. Deng, S.-M. Wang, T. Yin et al., “Dimethyl sulfoxide suppresses mouse 4T1 breast cancer growth by modulating tumor-associated macrophage differentiation,” Journal of Breast Cancer, vol. 17, no. 1, pp. 25–32, 2014. View at Publisher · View at Google Scholar · View at Scopus
  134. E. Van Overmeire, B. Stijlemans, F. Heymann et al., “M-CSF and GM-CSF receptor signaling differentially regulate monocyte maturation and macrophage polarization in the tumor microenvironment,” Cancer Research, vol. 76, no. 1, pp. 35–42, 2016. View at Publisher · View at Google Scholar · View at Scopus
  135. F. Ren, M. Fan, J. Mei et al., “Interferon-γ and celecoxib inhibit lung-tumor growth through modulating M2/M1 macrophage ratio in the tumor microenvironment,” Drug Design, Development and Therapy, vol. 8, pp. 1527–1538, 2014. View at Publisher · View at Google Scholar · View at Scopus
  136. R. Noy and J. Pollard, “Tumor-associated macrophages: from mechanisms to therapy,” Immunity, vol. 41, no. 1, pp. 49–61, 2014. View at Publisher · View at Google Scholar · View at Scopus
  137. Z. Guo, Z. Xing, X. Cheng et al., “Somatostatin derivate (smsDX) attenuates the TAM-stimulated proliferation, migration and invasion of prostate cancer via NF-κB regulation,” PLoS ONE, vol. 10, no. 5, Article ID e0124292, 2015. View at Publisher · View at Google Scholar
  138. H.-J. Choi, H.-J. Choi, T.-W. Chung, and K.-T. Ha, “Luteolin inhibits recruitment of monocytes and migration of Lewis lung carcinoma cells by suppressing chemokine (C-C motif) ligand 2 expression in tumor-associated macrophage,” Biochemical and Biophysical Research Communications, vol. 470, no. 1, pp. 101–106, 2016. View at Publisher · View at Google Scholar · View at Scopus