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The Scientific World Journal
Volume 2014 (2014), Article ID 521754, 14 pages
http://dx.doi.org/10.1155/2014/521754
Review Article

Transforming Growth Factor-Beta and Matrix Metalloproteinases: Functional Interactions in Tumor Stroma-Infiltrating Myeloid Cells

Laboratory for Experimental Hematology and Stem Cells, Institute for Medical Research, University of Belgrade, Dr Subotića 4, 11129 Belgrade, Serbia

Received 30 August 2013; Accepted 28 October 2013; Published 21 January 2014

Academic Editors: E. Ayroldi, D. Cataldo, and T. Quan

Copyright © 2014 Jelena Krstic and Juan F. Santibanez. 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. J. F. Santibañez, M. Quintanilla, and C. Bernabeu, “TGF-β/TGF-β receptor system and its role in physiological and pathological conditions,” Clinical Science, vol. 121, no. 6, pp. 233–251, 2011. View at Publisher · View at Google Scholar · View at Scopus
  2. B. Bierie and H. L. Moses, “TGF-β and cancer,” Cytokine and Growth Factor Reviews, vol. 17, no. 1-2, pp. 29–40, 2006. View at Publisher · View at Google Scholar · View at Scopus
  3. D. Padua and M. Massagué, “Roles of TGFbeta in metastasis,” Cell Research, vol. 19, no. 1, pp. 89–102, 2009. View at Google Scholar
  4. M. Quintanilla, G. del Castillo, J. Kocic, and J. F. . Santibanez, “TGF-B and MMPs: a complex regulatory loop involved in tumor progression,” in Matrix Metalloproteinases: Biology, Functions and Clinical Implications, N. Oshiro and E. Miyagi, Eds., Nova Science, 2012. View at Google Scholar
  5. D. G. Stover, B. Bierie, and H. L. Moses, “A delicate balance: TGF-β and the tumor microenvironment,” Journal of Cellular Biochemistry, vol. 101, no. 4, pp. 851–861, 2007. View at Publisher · View at Google Scholar · View at Scopus
  6. L. M. Wakefield and A. B. Roberts, “TGF-β signaling: positive and negative effects on tumorigenesis,” Current Opinion in Genetics and Development, vol. 12, no. 1, pp. 22–29, 2002. View at Publisher · View at Google Scholar · View at Scopus
  7. H. Hua, M. Li, T. Luo, Y. Yin, and Y. Jiang, “Matrix metalloproteinases in tumorigenesis: an evolving paradigm,” Cellular and Molecular Life Sciences, vol. 68, no. 23, pp. 3853–3868, 2011. View at Publisher · View at Google Scholar · View at Scopus
  8. C. Amălinei, I. D. Căruntu, S. E. Giuşcă, and R. A. Bălan, “Matrix metalloproteinases involvement in pathologic condition,” Romanian Journal of Morphology and Embryology, vol. 51, no. 2, pp. 215–228, 2010. View at Google Scholar
  9. M. Egeblad and Z. Werb, “New functions for the matrix metalloproteinases in cancer progression,” Nature Reviews Cancer, vol. 2, no. 3, pp. 161–174, 2002. View at Google Scholar · View at Scopus
  10. K. Kessenbrock, V. Plaks, and Z. Werb, “Matrix metalloproteinases: regulators of the tumor microenvironment,” Cell, vol. 141, no. 1, pp. 52–67, 2010. View at Publisher · View at Google Scholar · View at Scopus
  11. L. Attisano and J. L. Wrana, “Signal transduction by the TGF-β superfamily,” Science, vol. 296, no. 5573, pp. 1646–1647, 2002. View at Publisher · View at Google Scholar · View at Scopus
  12. Y. Shi and J. Massagué, “Mechanisms of TGF-β signaling from cell membrane to the nucleus,” Cell, vol. 113, no. 6, pp. 685–700, 2003. View at Publisher · View at Google Scholar · View at Scopus
  13. S. Itoh and P. ten Dijke, “Negative regulation of TGF-β receptor/Smad signal transduction,” Current Opinion in Cell Biology, vol. 19, no. 2, pp. 176–184, 2007. View at Publisher · View at Google Scholar · View at Scopus
  14. J. F. . Santibanez and J. Kocic, “Transforming growth factor-beta superfamily, implications in development and differentiation of stem cells,” BioMolecular Concepts, vol. 5, pp. 429–445, 2012. View at Google Scholar
  15. Y. Mu, S. K. Gudey, and M. Landström, “Non-Smad signaling pathways,” Cell and Tissue Research, vol. 347, no. 1, pp. 11–20, 2012. View at Publisher · View at Google Scholar · View at Scopus
  16. K. J. Gordon and G. C. Blobe, “Role of transforming growth factor-β superfamily signaling pathways in human disease,” Biochimica et Biophysica Acta, vol. 1782, no. 4, pp. 197–228, 2008. View at Publisher · View at Google Scholar · View at Scopus
  17. Z. Gatalica and E. Torlakovic, “Pathology of the hereditary colorectal carcinoma,” Familial Cancer, vol. 7, no. 1, pp. 15–26, 2008. View at Publisher · View at Google Scholar · View at Scopus
  18. J. Otten, C. Carsten Bokemeyer, and W. Fiedler, “TGF-β superfamily receptors—targets for antiangiogenic therapy?” Journal of Oncology, vol. 2010, Article ID 317068, 10 pages, 2010. View at Publisher · View at Google Scholar
  19. J. R. Howe, M. G. Sayed, A. F. Ahmed et al., “The prevalence of MADH4 and BMPR1A mutations in juvenile polyposis and absence of BMPR2, BMPR1B, and ACVR1 mutations,” Journal of Medical Genetics, vol. 41, no. 7, pp. 484–491, 2004. View at Google Scholar · View at Scopus
  20. K. Sweet, J. Willis, X.-P. Zhou et al., “Molecular classification of patients with unexplained hamartomatous and hyperplastic polyposis,” Journal of the American Medical Association, vol. 294, no. 19, pp. 2465–2473, 2005. View at Publisher · View at Google Scholar · View at Scopus
  21. K.-H. Shin, Y. J. Park, and J.-G. Park, “Mutational analysis of the transforming growth factor β receptor type II gene in hereditary nonpolyposis colorectal cancer and early-onset colorectal cancer patients,” Clinical Cancer Research, vol. 6, no. 2, pp. 536–540, 2000. View at Google Scholar · View at Scopus
  22. C. Millet and Y. E. Zhang, “Roles of Smad3 in TGF-β signaling during carcinogenesis,” Critical Reviews in Eukaryotic Gene Expression, vol. 17, no. 4, pp. 281–293, 2007. View at Google Scholar · View at Scopus
  23. R. L. Baldwin, H. Friess, M. Yokoyama et al., “Attenuated ALK5 receptor expression in human pancreatic cancer: correlation with resistance to growth inhibition,” International Journal of Cancer, vol. 67, no. 2, pp. 283–288, 1996. View at Publisher · View at Google Scholar
  24. R. A. Hinshelwood, L. I. Huschtscha, J. Melki et al., “Concordant epigenetic silencing of transforming growth factor-β signaling pathway genes occurs early in breast carcinogenesis,” Cancer Research, vol. 67, no. 24, pp. 11517–11527, 2007. View at Publisher · View at Google Scholar · View at Scopus
  25. S. Izumoto, N. Arita, T. Ohnishi et al., “Microsatellite instability and mutated type II transforming growth factor-β receptor gene in gliomas,” Cancer Letters, vol. 112, no. 2, pp. 251–256, 1997. View at Publisher · View at Google Scholar · View at Scopus
  26. R. B. Luwor, A. H. Kaye, and H.-J. Zhu, “Transforming growth factor-beta (TGF-β) and brain tumours,” Journal of Clinical Neuroscience, vol. 15, no. 8, pp. 845–855, 2008. View at Publisher · View at Google Scholar · View at Scopus
  27. C. Gialeli, A. D. Theocharis, and N. K. Karamanos, “Roles of matrix metalloproteinases in cancer progression and their pharmacological targeting,” The FEBS Journal, vol. 278, no. 1, pp. 16–27, 2011. View at Publisher · View at Google Scholar · View at Scopus
  28. S. Löffek, O. Schilling, and C.-W. Franzke, “Series “matrix metalloproteinases in lung health and disease”: biological role of matrix metalloproteinases: a critical balance,” European Respiratory Journal, vol. 38, no. 1, pp. 191–208, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. G. Murphy, “Tissue inhibitors of metalloproteinases,” Genome Biology, vol. 12, no. 11, article 233, 2011. View at Publisher · View at Google Scholar
  30. C. López-Otín and L. M. Matrisian, “Emerging roles of proteases in tumour suppression,” Nature Reviews Cancer, vol. 7, no. 10, pp. 800–808, 2007. View at Publisher · View at Google Scholar · View at Scopus
  31. J. P. Annes, J. S. Munger, and D. B. Rifkin, “Making sense of latent TGFβ activation,” Journal of Cell Science, vol. 116, no. 2, pp. 217–224, 2003. View at Publisher · View at Google Scholar · View at Scopus
  32. Q. Yu and I. Stamenkovic, “Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-β and promotes tumor invasion and angiogenesis,” Genes and Development, vol. 14, no. 2, pp. 163–176, 2000. View at Google Scholar · View at Scopus
  33. D. Mu, S. Cambier, L. Fjellbirkeland et al., “The integrin ανβ8 mediates epithelial homeostasis through MT1-MMP-dependent activation of TGF-β1,” Journal of Cell Biology, vol. 157, no. 3, pp. 493–507, 2002. View at Publisher · View at Google Scholar · View at Scopus
  34. L. D. Kerr, D. B. Miller, and L. M. Matrisian, “TGF-β1 inhibition of transin/stromelysin gene expression is mediated through a fos binding sequence,” Cell, vol. 61, no. 2, pp. 267–278, 1990. View at Publisher · View at Google Scholar · View at Scopus
  35. S. Narayan, T. Thangasamy, and R. Balusu, “Transforming growth factor -beta receptor signaling in cancer,” Frontiers in Bioscience, vol. 10, pp. 1135–1145, 2005. View at Google Scholar · View at Scopus
  36. L. Zawel, J. Le Dai, P. Buckhaults et al., “Human Smad3 and Smad4 are sequence-specific transcription activators,” Molecular Cell, vol. 1, no. 4, pp. 611–617, 1998. View at Google Scholar · View at Scopus
  37. E. Hijova, “Matrix metalloproteinases: their biological functions and clinical implications,” Bratislavske Lekarske Listy, vol. 106, no. 3, pp. 127–132, 2005. View at Google Scholar · View at Scopus
  38. C.-S. Lin and C.-H. Pan, “Regulatory mechanisms of atrial fibrotic remodeling in atrial fibrillation,” Cellular and Molecular Life Sciences, vol. 65, no. 10, pp. 1489–1508, 2008. View at Publisher · View at Google Scholar · View at Scopus
  39. L. A. White, T. I. Mitchell, and C. E. Brinckerhoff, “Transforming growth factor β inhibitory element in the rabbit matrix metalloproteinase-1 (collagenase-1) gene functions as a repressor of constitutive transcription,” Biochimica et Biophysica Acta, vol. 1490, no. 3, pp. 259–268, 2000. View at Publisher · View at Google Scholar · View at Scopus
  40. W. Yuan and J. Varga, “Transforming growth factor-β repression of matrix metalloproteinase-1 in dermal fibroblasts involves Smad3,” Journal of Biological Chemistry, vol. 276, no. 42, pp. 38502–38510, 2001. View at Publisher · View at Google Scholar · View at Scopus
  41. M. Gaire, Z. Magbanua, S. McDonnell, L. McNeil, D. H. Lovett, and L. M. Matrisian, “Structure and expression of the human gene for the matrix metalloproteinase matrilysin,” Journal of Biological Chemistry, vol. 269, no. 3, pp. 2032–2040, 1994. View at Google Scholar · View at Scopus
  42. K. Ogawa, F. Chen, C. Kuang, and Y. Chen, “Suppression of matrix metalloproteinase-9 transcription by transforming growth factor-β is mediated by a nuclear factor-κB site,” The Biochemical Journal, vol. 381, no. 2, pp. 413–422, 2004. View at Publisher · View at Google Scholar · View at Scopus
  43. G. Tardif, P. Reboul, M. Dupuis et al., “Transforming growth factor-β induced collagenase-3 production in human osteoarthritic chondrocytes is triggered by smad proteins: cooperation between activator protein-1 and PEA-3 binding sites,” Journal of Rheumatology, vol. 28, no. 7, pp. 1631–1639, 2001. View at Google Scholar · View at Scopus
  44. J. Lohi, K. Lehti, H. Valtanen, W. C. Parks, and J. Keski-Oja, “Structural analysis and promoter characterization of the human membrane-type matrix metalloproteinase-1 (MT1-MMP) gene,” Gene, vol. 242, no. 1-2, pp. 75–86, 2000. View at Publisher · View at Google Scholar · View at Scopus
  45. F. Ishikawa, H. Miyoshi, K. Nose, and M. Shibanuma, “Transcriptional induction of MMP-10 by TGF-Β, mediated by activation of MEF2A and downregulation of class IIa HDACs,” Oncogene, vol. 29, no. 6, pp. 909–919, 2010. View at Publisher · View at Google Scholar · View at Scopus
  46. N. T. Liberati, M. B. Datto, J. P. Frederick et al., “Smads bind directly to the Jun family of AP-1 transcription factors,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 9, pp. 4844–4849, 1999. View at Publisher · View at Google Scholar · View at Scopus
  47. F. Verrecchia, L. Vindevoghel, R. J. Lechleider, J. Uitto, A. B. Roberts, and A. Mauviel, “Smad3/AP-1 interactions control transcriptional responses to TGF-β in a promoter-specific manner,” Oncogene, vol. 20, no. 26, pp. 3332–3340, 2001. View at Publisher · View at Google Scholar · View at Scopus
  48. N. Selvamurugan, S. Kwok, and N. C. Partridge, “Smad3 interacts with JunB and Cbfa1/Runx2 for transforming growth factor-β1-stimulated collagenase-3 expression in human breast cancer cells,” Journal of Biological Chemistry, vol. 279, no. 26, pp. 27764–27773, 2004. View at Publisher · View at Google Scholar · View at Scopus
  49. M. E. Fini, J. R. Cook, R. Mohan, and C. E. Brinckerhoff, “Regulation of matrix metalloproteinase gene expression,” in Matrix Metalloproteinases, W. C. Parks and R. P. Mecham, Eds., pp. 299–359, Academic Press, New York, NY, USA, 1988. View at Google Scholar
  50. C. Yan and D. D. Boyd, “Regulation of matrix metalloproteinase expression expression,” Journal of Cellular Physiology, vol. 211, no. 1, pp. 19–26, 2007. View at Publisher · View at Google Scholar · View at Scopus
  51. A. Mauviel, K.-Y. Chung, A. Agarwal, K. Tamai, and J. Uitto, “Cell-specific induction of distinct oncogenes of the jun family is responsible for differential regulation of collagenase gene expression by transforming growth factor-β in fibroblasts and keratinocytes,” Journal of Biological Chemistry, vol. 271, no. 18, pp. 10917–10923, 1996. View at Publisher · View at Google Scholar · View at Scopus
  52. E.-S. Kim, Y.-W. Sohn, and A. Moon, “TGF-β-induced transcriptional activation of MMP-2 is mediated by activating transcription factor (ATF)2 in human breast epithelial cells,” Cancer Letters, vol. 252, no. 1, pp. 147–156, 2007. View at Publisher · View at Google Scholar · View at Scopus
  53. Y. Sano, J. Harada, S. Tashiro, R. Gotoh-Mandeville, T. Maekawa, and S. Ishii, “ATF-2 is a common nuclear target of smad and TAK1 pathways in transforming growth factor-β signaling,” Journal of Biological Chemistry, vol. 274, no. 13, pp. 8949–8957, 1999. View at Publisher · View at Google Scholar · View at Scopus
  54. M. G. Binker, A. A. Binker-Cosen, H. Y. Gaisano, R. H. de Cosen, and L. I. Cosen-Binker, “TGF-β1 increases invasiveness of SW1990 cells through Rac1/ROS/NF-κB/IL-6/MMP-2,” Biochemical and Biophysical Research Communications, vol. 405, no. 1, pp. 140–145, 2011. View at Publisher · View at Google Scholar · View at Scopus
  55. J. F. Santibanez, J. Guerrero, M. Quintanilla, A. Fabra, and J. Martínez, “Transforming growth factor-β1 modulates matrix metalloproteinase-9 production through the Ras/MAPK signaling pathway in transformed keratinocytes,” Biochemical and Biophysical Research Communications, vol. 296, no. 2, pp. 267–273, 2002. View at Publisher · View at Google Scholar · View at Scopus
  56. N. Tobar, V. Villar, and J. F. Santibanez, “ROS-NFκΒ mediates TGF-β1-induced expression of urokinase-type plasminogen activator, matrix metalloproteinase-9 and cell invasion,” Molecular and Cellular Biochemistry, vol. 340, no. 1-2, pp. 195–202, 2010. View at Publisher · View at Google Scholar · View at Scopus
  57. A. Safina, E. Vandette, and A. V. Bakin, “ALK5 promotes tumor angiogenesis by upregulating matrix metalloproteinase-9 in tumor cells,” Oncogene, vol. 26, no. 17, pp. 2407–2422, 2007. View at Publisher · View at Google Scholar · View at Scopus
  58. M. Arsura, G. R. Panta, J. D. Bilyeu et al., “Transient activation of NF-κB through a TAK1/IKK kinase pathway by TGF-β1 inhibits AP-1/SMAD signaling and apoptosis: implications in liver tumor formation,” Oncogene, vol. 22, no. 3, pp. 412–425, 2003. View at Publisher · View at Google Scholar · View at Scopus
  59. A. Safina, M.-Q. Ren, E. Vandette, and A. V. Bakin, “TAK1 is required for TGF-β1-mediated regulation of matrix metalloproteinase-9 and metastasis,” Oncogene, vol. 27, no. 9, pp. 1198–1207, 2008. View at Publisher · View at Google Scholar · View at Scopus
  60. R. M. Bremnes, T. Dønnem, S. Al-Saad et al., “The role of tumor stroma in cancer progression and prognosis: emphasis on carcinoma-associated fibroblasts and non-small cell lung cancer,” Journal of Thoracic Oncology, vol. 6, no. 1, pp. 209–217, 2011. View at Publisher · View at Google Scholar · View at Scopus
  61. L. A. Liotta and E. C. Kohn, “The microenvironment of the tumour: host interface,” Nature, vol. 411, no. 6835, pp. 375–379, 2001. View at Publisher · View at Google Scholar · View at Scopus
  62. C. C. Park, M. J. Bissell, and M. H. Barcellos-Hoff, “The influence of the microenvironment on the malignant phenotype,” Molecular Medicine Today, vol. 6, no. 8, pp. 324–329, 2000. View at Publisher · View at Google Scholar · View at Scopus
  63. S. M. Ansell and R. H. Vonderheide, “Cellular composition of the tumor microenvironment,” in American Society of Clinical Oncology Educational Book, vol. 2013, pp. 91–97, 2013. View at Google Scholar
  64. M. Hu and K. Polyak, “Microenvironmental regulation of cancer development,” Current Opinion in Genetics and Development, vol. 18, no. 1, pp. 27–34, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. A. Noël, M. Jost, and E. Maquoi, “Matrix metalloproteinases at cancer tumor-host interface,” Seminars in Cell and Developmental Biology, vol. 19, no. 1, pp. 52–60, 2008. View at Publisher · View at Google Scholar · View at Scopus
  66. G. Han, F. Li, T. P. Singh et al., “The pro-inflammatory role of TGFβ1: a paradox?” International Journal of Biological Sciences, vol. 8, no. 2, pp. 228–235, 2012. View at Google Scholar
  67. H. F. Dvorak, “Tumors: wounds that do not heal: similarities between tumor stroma generation and wound healing,” The New England Journal of Medicine, vol. 315, no. 26, pp. 1650–1659, 1986. View at Google Scholar · View at Scopus
  68. T. L. Whiteside, “The tumor microenvironment and its role in promoting tumor growth,” Oncogene, vol. 27, no. 45, pp. 5904–5912, 2008. View at Publisher · View at Google Scholar · View at Scopus
  69. P. Allavena, C. Garlanda, M. G. Borrello, A. Sica, and A. Mantovani, “Pathways connecting inflammation and cancer,” Current Opinion in Genetics and Development, vol. 18, no. 1, pp. 3–10, 2008. View at Publisher · View at Google Scholar · View at Scopus
  70. 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
  71. P. Allavena, A. Sica, G. Solinas, C. Porta, and A. Mantovani, “The inflammatory micro-environment in tumor progression: the role of tumor-associated macrophages,” Critical Reviews in Oncology/Hematology, vol. 66, no. 1, pp. 1–9, 2008. View at Publisher · View at Google Scholar · View at Scopus
  72. A. Yoshimura, Y. Wakabayashi, and T. Mori, “Cellular and molecular basis for the regulation of inflammation by TGF-β,” Journal of Biochemistry, vol. 147, no. 6, pp. 781–792, 2010. View at Publisher · View at Google Scholar · View at Scopus
  73. A. M. Manicone and J. K. McGuire, “Matrix metalloproteinases as modulators of inflammation,” Seminars in Cell and Developmental Biology, vol. 19, no. 1, pp. 34–41, 2008. View at Publisher · View at Google Scholar · View at Scopus
  74. S. Ueha, F. H. W. Shand, and K. Matsushima, “Myeloid cell population dynamics in healthy and tumor-bearing mice,” International Immunopharmacology, vol. 11, no. 7, pp. 783–788, 2011. View at Publisher · View at Google Scholar · View at Scopus
  75. A. D. Kennedy and F. R. DeLeo, “Neutrophil apoptosis and the resolution of infection,” Immunologic Research, vol. 43, no. 1–3, pp. 25–61, 2009. View at Google Scholar
  76. O. Soehnlein, C. Weber, and L. Lindbom, “Neutrophil granule proteins tune monocytic cell function,” Trends in Immunology, vol. 30, no. 11, pp. 538–546, 2009. View at Publisher · View at Google Scholar · View at Scopus
  77. L. Bingle, N. J. Brown, and C. E. Lewis, “The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies,” Journal of Pathology, vol. 196, no. 3, pp. 254–265, 2002. View at Publisher · View at Google Scholar · View at Scopus
  78. A. Zumsteg and G. Christofori, “Corrupt policemen: inflammatory cells promote tumor angiogenesis,” Current Opinion in Oncology, vol. 21, no. 1, pp. 60–70, 2009. View at Publisher · View at Google Scholar · View at Scopus
  79. T. Hagemann, J. Wilson, F. Burke et al., “Ovarian cancer cells polarize macrophages toward a tumor-associated phenotype,” Journal of Immunology, vol. 176, no. 8, pp. 5023–5032, 2006. View at Google Scholar · View at Scopus
  80. D. G. DeNardo, J. B. Barreto, P. Andreu et al., “CD4+ T cells regulate pulmonary metastasis of mammary carcinomas by enhancing protumor properties of macrophages,” Cancer Cell, vol. 16, no. 2, pp. 91–102, 2009. View at Publisher · View at Google Scholar · View at Scopus
  81. 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
  82. A. Mantovani and M. Locati, “Tumor-associated macrophages as a paradigm of macrophage plasticity, diversity, and polarization: lessons and open questions,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 33, no. 7, pp. 1478–1483, 2013. View at Publisher · View at Google Scholar
  83. 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
  84. N. B. Hao, M. H. Lü, Y. H. Fan et al., “Macrophages in tumor microenvironments and the progression of tumors,” Clinical and Developmental Immunology, vol. 2012, Article ID 948098, 11 pages, 2012. View at Publisher · View at Google Scholar
  85. E. Obermueller, S. Vosseler, N. E. Fusenig, and M. M. Mueller, “Cooperative autocrine and paracrine functions of granulocyte colony-stimulating factor and granulocyte-macrophage colony-stimulating factor in the progression of skin carcinoma cells,” Cancer Research, vol. 64, no. 21, pp. 7801–7812, 2004. View at Publisher · View at Google Scholar · View at Scopus
  86. 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
  87. J. Wyckoff, W. Wang, E. Y. Lin et al., “A paracrine loop between tumor cells and macrophages is required for tumor cell migration in mammary tumors,” Cancer Research, vol. 64, no. 19, pp. 7022–7029, 2004. View at Publisher · View at Google Scholar · View at Scopus
  88. P. P. McDonald, V. A. Fadok, D. Bratton, and P. M. Henson, “Transcriptional and translational regulation of inflammatory mediator production by endogenous TGF-β in macrophages that have ingested apoptotic cells,” Journal of Immunology, vol. 163, no. 11, pp. 6164–6172, 1999. View at Google Scholar · View at Scopus
  89. 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
  90. A. M. Houghton, J. L. Grisolano, M. L. Baumann et al., “Macrophage elastase (matrix metalloproteinase-12) suppresses growth of lung metastases,” Cancer Research, vol. 66, no. 12, pp. 6149–6155, 2006. View at Publisher · View at Google Scholar · View at Scopus
  91. M. W. Feinberg, M. K. Jain, F. Werner et al., “Transforming growth factor-β1 inhibits cytokine-mediated induction of human metalloelastase in macrophages,” Journal of Biological Chemistry, vol. 275, no. 33, pp. 25766–25773, 2000. View at Publisher · View at Google Scholar · View at Scopus
  92. S.-H. Jeon, B.-C. Chae, H.-A. Kim et al., “Mechanisms underlying TGF-β1-induced expression of VEGF and Flk-1 in mouse macrophages and their implications for angiogenesis,” Journal of Leukocyte Biology, vol. 81, no. 2, pp. 557–566, 2007. View at Publisher · View at Google Scholar · View at Scopus
  93. S. V. Novitskiy, M. W. Pickup, A. Chytil et al., “Deletion of TGF-beta signaling in myeloid cells enhances their anti-tumorigenic properties,” Journal of Leukocyte Biology, vol. 92, no. 3, pp. 641–651, 2012. View at Publisher · View at Google Scholar
  94. 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
  95. Z. G. Fridlender and S. M. Albelda, “Tumor-associated neutrophils: friend or foe?” Carcinogenesis, vol. 33, no. 5, pp. 949–955, 2012. View at Publisher · View at Google Scholar · View at Scopus
  96. A. Mantovani, M. A. Cassatella, C. Costantini, and S. Jaillon, “Neutrophils in the activation and regulation of innate and adaptive immunity,” Nature Reviews Immunology, vol. 11, no. 8, pp. 519–531, 2011. View at Publisher · View at Google Scholar · View at Scopus
  97. M. R. Galdiero, C. Garlanda, S. Jaillon et al., “Tumor associated macrophages and neutrophils in tumor progression,” Journal of Cellular Physiology, vol. 228, no. 7, pp. 1404–1412, 2013. View at Publisher · View at Google Scholar
  98. 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
  99. 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
  100. Z. G. Fridlender, J. Sun, S. Kim et al., “Polarization of tumor-associated neutrophil phenotype by TGF-β: “N1” versus “N2” TAN,” Cancer Cell, vol. 16, no. 3, pp. 183–194, 2009. View at Publisher · View at Google Scholar · View at Scopus
  101. L. A. Pekarek, B. A. Starr, A. Y. Toledano, and H. Schreiber, “Inhibition of tumor growth by elimination of granulocytes,” Journal of Experimental Medicine, vol. 181, no. 1, pp. 435–440, 1995. View at Publisher · View at Google Scholar · View at Scopus
  102. A. Mantovani, “The Yin-Yang of tumor-associated neutrophils,” Cancer Cell, vol. 16, no. 3, pp. 173–174, 2009. View at Publisher · View at Google Scholar · View at Scopus
  103. J.-J. Chen, Y. Sun, and G. J. Nabel, “Regulation of the proinflammatory effects of Fas ligand (CD95L),” Science, vol. 282, no. 5394, pp. 1714–1717, 1998. View at Google Scholar · View at Scopus
  104. H. B. Acuff, K. J. Carter, B. Fingleton, D. L. Gorden, and L. M. Matrisian, “Matrix metalloproteinase-9 from bone marrow-derived cells contributes to survival but not growth of tumor cells in the lung microenvironment,” Cancer Research, vol. 66, no. 1, pp. 259–266, 2006. View at Publisher · View at Google Scholar · View at Scopus
  105. K. J. Balazovich, R. Fernandez, V. Hinkovska-Galcheva, S. J. Suchard, and L. A. Boxer, “Transforming growth factor-β1 stimulates degranulation and oxidant release by adherent human neutrophils,” Journal of Leukocyte Biology, vol. 60, no. 6, pp. 772–777, 1996. View at Google Scholar · View at Scopus
  106. J. E. De Larco, B. R. K. Wuertz, and L. T. Furcht, “The potential role of neutrophils in promoting the metastatic phenotype of tumors releasing interleukin-8,” Clinical Cancer Research, vol. 10, no. 15, pp. 4895–4900, 2004. View at Publisher · View at Google Scholar · View at Scopus
  107. C. López-Otín, L. H. Palavalli, and Y. Samuels, “Protective roles of matrix metalloproteinases: from mouse models to human cancer,” Cell Cycle, vol. 8, no. 22, pp. 3657–3662, 2009. View at Publisher · View at Google Scholar · View at Scopus
  108. M. Balbín, A. Fueyo, A. M. Tester et al., “Loss of collagenase-2 confers increased skin tumor susceptibility to male mice,” Nature Genetics, vol. 35, no. 3, pp. 252–257, 2003. View at Publisher · View at Google Scholar · View at Scopus
  109. H. Palosaari, J. Wahlgren, M. Larmas et al., “The expression of MMP-8 in human odontoblasts and dental pulp cells is down-regulated by TGF-β1,” Journal of Dental Research, vol. 79, no. 1, pp. 77–84, 2000. View at Google Scholar · View at Scopus
  110. M. Yang, H. Shen, C. Qiu et al., “High expression of miR-21 and miR-155 predicts recurrence and unfavourable survival in non-small cell lung cancer,” European Journal of Cancer, vol. 49, no. 3, pp. 604–615, 2013. View at Publisher · View at Google Scholar
  111. J. Zavadil, M. Narasimhan, M. Blumenberg, and R. J. Schneider, “Transforming growth factor-β and microRNA:mRNA regulatory networks in epithelial plasticity,” Cells Tissues Organs, vol. 185, no. 1–3, pp. 157–161, 2007. View at Publisher · View at Google Scholar · View at Scopus
  112. C. Soria-Valles, A. Gutiérrez-Fernández, M. Guiu et al., “The anti-metastatic activity of collagenase-2 in breast cancer cells is mediated by a signaling pathway involving decorin and miR-21,” Oncogene, 2013. View at Publisher · View at Google Scholar
  113. K. M. Hargadon, “Tumor-altered dendritic cell function: implications for anti-tumor immunity,” Frontiers in Immunology, vol. 4, article 192, 2013. View at Publisher · View at Google Scholar
  114. K. Bauer, S. Michel, M. Reuschenbach, N. Nelius, M. Von Knebel Doeberitz, and M. Kloor, “Dendritic cell and macrophage infiltration in microsatellite-unstable and microsatellite-stable colorectal cancer,” Familial Cancer, vol. 10, no. 3, pp. 557–565, 2011. View at Publisher · View at Google Scholar · View at Scopus
  115. F. Ghiringhelli, P. E. Puig, S. Roux et al., “Tumor cells convert immature myeloid dendritic cells into TGF-β-secreting cells inducing CD4+CD25+ regulatory T cell proliferation,” Journal of Experimental Medicine, vol. 202, no. 7, pp. 919–929, 2005. View at Publisher · View at Google Scholar · View at Scopus
  116. S. H. Wrzesinski, Y. Y. Wan, and R. A. Flavell, “Transforming growth factor-β and the immune response: implications for anticancer therapy,” Clinical Cancer Research, vol. 13, no. 18, part 1, pp. 5262–5270, 2007. View at Publisher · View at Google Scholar · View at Scopus
  117. F. Geissmann, P. Revy, A. Regnault et al., “TGF-β1 prevents the noncognate maturation of human dendritic Langerhans cells,” Journal of Immunology, vol. 162, no. 8, pp. 4567–4575, 1999. View at Google Scholar · View at Scopus
  118. P. Chaux, N. Favre, B. Bonnotte, M. Moutet, M. Martin, and F. Martin, “Tumor-infiltrating dendritic cells are defective in their antigen-presenting function and inducible B7 expression. A role in the immune tolerance to antigenic tumors,” Advances in Experimental Medicine and Biology, vol. 417, pp. 525–528, 1997. View at Google Scholar · View at Scopus
  119. K. Kis-Toth, I. Bacskai, P. Gogolak et al., “Monocyte-derived dendritic cell subpopulations use different types of matrix metalloproteinases inhibited by GM6001,” Immunobiology, vol. 218, no. 11, pp. 1361–1369, 2013. View at Publisher · View at Google Scholar
  120. C. Gawden-Bone, Z. Zhou, E. King, A. Prescott, C. Watts, and J. Lucocq, “Dendritic cell podosomes are protrusive and invade the extracellular matrix using metalloproteinase MMP-14,” Journal of Cell Science, vol. 123, part 9, pp. 1427–1437, 2010. View at Publisher · View at Google Scholar · View at Scopus
  121. D. Ribatti, “Mast cells and macrophages exert beneficial and detrimental effects on tumor progression and angiogenesis,” Immunology Letters, vol. 152, no. 2, pp. 83–88, 2013. View at Publisher · View at Google Scholar
  122. D. Ribatti and E. Crivellato, “The controversial role of mast cells in tumor growth,” International Review of Cell and Molecular Biology, vol. 275, no. C, pp. 89–131, 2009. View at Publisher · View at Google Scholar · View at Scopus
  123. B. L. Gruber, M. J. Marchese, and R. R. Kew, “Transforming growth factor-β1 mediates mast cell chemotaxis,” Journal of Immunology, vol. 152, no. 12, pp. 5860–5867, 1994. View at Google Scholar · View at Scopus
  124. G. Dyduch, K. Kaczmarczyk, and K. Okoń, “Mast cells and cancer: enemies or allies?” Polish Journal of Pathology, vol. 63, no. 1, pp. 1–7, 2012. View at Google Scholar · View at Scopus
  125. 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
  126. K. Ganeshan and P. J. Bryce, “Regulatory T cells enhance mast cell production of IL-6 via surface-bound TGF-β,” Journal of Immunology, vol. 188, no. 2, pp. 594–603, 2012. View at Publisher · View at Google Scholar · View at Scopus
  127. A. S. Chung, X. Wu, G. Zhuang et al., “An interleukin-17-mediated paracrine network promotes tumor resistance to anti-angiogenic therapy,” Nature Medicine, vol. 19, pp. 1114–1123, 2013. View at Publisher · View at Google Scholar
  128. W. C. Chen, Y. H. Lai, H. Y. Chen et al., “Interleukin-17-producing cell infiltration in the breast cancer tumor microenvironment is a poor prognostic factor,” Histopathology, vol. 63, no. 2, pp. 225–233, 2013. View at Google Scholar
  129. J.-S. Nam, M. Terabe, M.-J. Kang et al., “Transforming growth factor β subverts the immune system into directly promoting tumor growth through interleukin-17,” Cancer Research, vol. 68, no. 10, pp. 3915–3923, 2008. View at Publisher · View at Google Scholar · View at Scopus
  130. M. Numasaki, J.-I. Fukushi, M. Ono et al., “Interleukin-17 promotes angiogenesis and tumor growth,” Blood, vol. 101, no. 7, pp. 2620–2627, 2003. View at Publisher · View at Google Scholar · View at Scopus
  131. 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
  132. 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
  133. W. R. Roche, “The nature and significance of tumour-associated mast cells,” Journal of Pathology, vol. 148, no. 2, pp. 175–182, 1986. View at Google Scholar · View at Scopus
  134. K. C. Fang, P. J. Wolters, M. Steinhoff, A. Bidgol, J. L. Blount, and G. H. Caughey, “Mast cell expression of gelatinases A and B is regulated by kit ligand and TGF-β,” Journal of Immunology, vol. 162, no. 9, pp. 5528–5535, 1999. View at Google Scholar · View at Scopus
  135. B. L. Gruber, M. J. Marchese, K. Suzuki et al., “Synovial procollagenase activation by human mast cell tryptase dependence upon matrix metalloproteinase 3 activation,” Journal of Clinical Investigation, vol. 84, no. 5, pp. 1657–1662, 1989. View at Google Scholar · View at Scopus
  136. A. Dufour, “Overall CM missing the target: matrix metalloproteinase antitargets in inflammation and cancer,” Trends in Pharmacological Sciences, vol. 34, no. 4, pp. 233–242, 2013. View at Publisher · View at Google Scholar
  137. W. Zhang, X.-D. Zhu, H.-C. Sun et al., “Depletion of tumor-associated macrophages enhances the effect of sorafenib in metastatic liver cancer models by antimetastatic and antiangiogenic effects,” Clinical Cancer Research, vol. 16, no. 13, pp. 3420–3430, 2010. View at Publisher · View at Google Scholar · View at Scopus
  138. J. Vukanovic and J. T. Isaacs, “Linomide inhibits angiogenesis, growth, metastasis, and macrophage infiltration within rat prostatic cancers,” Cancer Research, vol. 55, no. 7, pp. 1499–1504, 1995. View at Google Scholar · View at Scopus
  139. S. Zhu, M. Niu, H. O. 'Mary, and Z. Cui, “Targeting of tumor-associated macrophages made possible by PEG-sheddable, mannose-modified nanoparticles,” Molecular Pharmaceutics, vol. 10, no. 9, pp. 3525–3530, 2013. View at Publisher · View at Google Scholar