Tumour hypoxia promotes melanoma growth and metastasis via High Mobility Group Box-1 and M2-like macrophages

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Huber, Roman ^a   Meier, Barbara ^a   Otsuka, Atsushi ^a   Fenini, Gabriele ^a   Satoh, Takashi ^a   Gehrke, Samuel ^a   Widmer, Daniel ^a   Levesque, Mitchell P ^a   Mangana, Joanna ^a   Kerl, Katrin ^a   Gebhardt, Christoffer ^b,c   Fujii, Hiroko ^d   Nakashima, Chisa ^d   Nonomura, Yumi ^d   Kabashima, Kenji ^d   Dummer, Reinhard ^a   Contassot, Emmanuel ^a   French, Lars E ^a  

^a UNIVERSITY HOSPITAL ZURICH   (Switzerland)

^b GERMAN CANCER RESEARCH CENTER DKFZ   (Germany)

^c UNIVERSITY OF HEIDELBERG   (Germany)

^d KYOTO UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ADVANCED GLYCATION END PRODUCT RECEPTOR; HIGH MOBILITY GROUP B1 PROTEIN; HYPOXIA INDUCIBLE FACTOR 1ALPHA; INTERLEUKIN 10;

ANIMAL; BLOOD; C57BL MOUSE; CELL PROLIFERATION; EXPERIMENTAL MELANOMA; FEMALE; HUMAN; MACROPHAGE; MALE; METABOLISM; PATHOLOGY; PHENOTYPE; SKIN TUMOR; TUMOR HYPOXIA;

ANIMALS; CELL PROLIFERATION; FEMALE; HMGB1 PROTEIN; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; INTERLEUKIN-10; MACROPHAGES; MALE; MELANOMA, EXPERIMENTAL; MICE, INBRED C57BL; PHENOTYPE; RECEPTOR FOR ADVANCED GLYCATION END PRODUCTS; SKIN NEOPLASMS; TUMOR HYPOXIA;

EID: 84978906776     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep29914     Document Type: Article

References (58)

1. Harris A. L. Hypoxia-A key regulatory factor in tumour growth. Nat Rev Cancer 2, 38-47 (2002).
2. Vaupel P, & Mayer A. Hypoxia in cancer: significance and impact on clinical outcome. Cancer Metastasis Rev 26, 225-239 (2007).
3. Vaupel P, Kallinowski F, & Okunieff P. Blood flow, oxygen and nutrient supply, and metabolic microenvironment of human tumours: a review. Cancer Res 49, 6449-6465 (1989).
4. Sims G. P, Rowe D. C, Rietdijk S. T, Herbst R, & Coyle A. J. HMGB1 and RAGE in inflammation and cancer. Annu Rev Immunol 28, 367-388 (2010).
5. Agresti A, & Bianchi M. E. HMGB proteins and gene expression. Curr Opin Genet Dev 13, 170-178 (2003).
6. Bianchi M. E, Beltrame M, & Paonessa G. Specific recognition of cruciform DNA by nuclear protein HMG1. Science 243, 1056-1059 (1989).
7. Ibrahim Z. A, Armour C. L, Phipps S, & Sukkar M. B. RAGE and TLRs: relatives, friends or neighbours?. Mol Immunol 56, 739-744 (2013).
8. Andersson U, & Tracey K. J. HMGB1 is a therapeutic target for sterile inflammation and infection. Annu Rev Immunol 29, 139-162 (2011).
9. Bianchi M. E. HMGB1 loves company. J Leukoc Biol 86, 573-576 (2009).
10. Carbone M, et al. Erionite exposure in North Dakota and Turkish villages with mesothelioma. Proc Natl Acad Sci USA 108, 13618-13623 (2011).
11. Jube S, et al. Cancer cell secretion of the DAMP protein HMGB1 supports progression in malignant mesothelioma. Cancer Res 72, 3290-3301 (2012).
12. Yang H, et al. Programmed necrosis induced by asbestos in human mesothelial cells causes high-mobility group box 1 protein release and resultant inflammation. Proc Natl Acad Sci USA 107, 12611-12616 (2010).
13. Liu Y, et al. Hypoxia induced HMGB1 and mitochondrial DNA interactions mediate tumour growth in hepatocellular carcinoma through Toll Like Receptor 9. J Hepatol 63, 114-121 (2015).
14. Gebhardt C, et al. RAGE signalling sustains inflammation and promotes tumour development. J Exp Med 205, 275-285 (2008).
15. Mittal D, et al. TLR4-mediated skin carcinogenesis is dependent on immune and radioresistant cells. Embo J 29, 2242-2252 (2010).
16. Hockel M, et al. Association between tumour hypoxia and malignant progression in advanced cancer of the uterine cervix. Cancer Res 56, 4509-4515 (1996).
17. Hanahan D, & Weinberg R. A. The hallmarks of cancer. Cell 100, 57-70 (2000).
18. Semenza G. L. Cancer-stromal cell interactions mediated by hypoxia-inducible factors promote angiogenesis, lymphangiogenesis, and metastasis. Oncogene 32, 4057-4063 (2013).
19. Sica A, Schioppa T, Mantovani A, & Allavena P. Tumour-Associated macrophages are a distinct M2 polarised population promoting tumour progression: potential targets of anti-cancer therapy. Eur J Cancer 42, 717-727 (2006).
20. Mantovani A, & Sica A. Macrophages, innate immunity and cancer: balance, tolerance, and diversity. Curr Opin Immunol 22, 231-237 (2010).
21. Talmadge J. E, Donkor M, & Scholar E. Inflammatory cell infiltration of tumours: Jekyll or Hyde. Cancer Metastasis Rev 26, 373-400 (2007).
22. Biswas S. K, & Mantovani A. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat Immunol 11, 889-896 (2010).
23. Ruffell B, Affara N. I, & Coussens L. M. Differential macrophage programming in the tumour microenvironment. Trends Immunol 33, 119-126 (2012).
24. Qian B. Z, & Pollard J. W. Macrophage diversity enhances tumour progression and metastasis. Cell 141, 39-51 (2010).
25. Tsung A, et al. HMGB1 release induced by liver ischemia involves Toll-like receptor 4 dependent reactive oxygen species production and calcium-mediated signalling. J Exp Med 204, 2913-2923 (2007).
26. Rofstad E. K, & Danielsen T. Hypoxia-induced angiogenesis and vascular endothelial growth factor secretion in human melanoma. Br J Cancer 77, 897-902 (1998).
27. Mantovani A, et al. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25, 677-686 (2004).
28. Liu G, et al. Phenotypic and functional switch of macrophages induced by regulatory CD4 + CD25+ T cells in mice. Immunol Cell Biol 89, 130-142 (2011).
29. Wan L, Pantel K, & Kang Y. Tumour metastasis: moving new biological insights into the clinic. Nat Med 19, 1450-1464 (2013).
30. Joyce J. A, & Pollard J. W. Microenvironmental regulation of metastasis. Nat Rev Cancer 9, 239-252 (2009).
31. Siveen K. S, & Kuttan G. Role of macrophages in tumour progression. Immunol Lett 123, 97-102 (2009).
32. Farinha P, et al. Analysis of multiple biomarkers shows that lymphoma-Associated macrophage (LAM) content is an independent predictor of survival in follicular lymphoma (FL). Blood 106, 2169-2174 (2005).
33. Hanada T, et al. Prognostic value of tumour-Associated macrophage count in human bladder cancer. Int J Urol 7, 263-269 (2000).
34. Steidl C, et al. Tumour-Associated macrophages and survival in classic Hodgkin's lymphoma. N Engl J Med 362, 875-885 (2010).
35. Zhu X. D, et al. High expression of macrophage colony-stimulating factor in peritumoural liver tissue is associated with poor survival after curative resection of hepatocellular carcinoma. J Clin Oncol 26, 2707-2716 (2008).
36. Chai C. Y, et al. Hypoxia-inducible factor-1alpha expression correlates with focal macrophage infiltration, angiogenesis and unfavourable prognosis in urothelial carcinoma. J Clin Pathol 61, 658-664 (2008).
37. Laoui D, et al. Tumour hypoxia does not drive differentiation of tumour-Associated macrophages but rather fine-Tunes the M2-like macrophage population. Cancer Res 74, 24-30 (2014).
38. Lima L, et al. The predominance of M2-polarized macrophages in the stroma of low-hypoxic bladder tumours is associated with BCG immunotherapy failure. Urol Oncol 32, 449-457 (2014).
39. Murdoch C, & Lewis C. E. Macrophage migration and gene expression in response to tumour hypoxia. Int J Cancer 117, 701-708 (2005).
40. Murdoch C, Muthana M, Coffelt S. B, & Lewis C. E. The role of myeloid cells in the promotion of tumour angiogenesis. Nat Rev Cancer 8, 618-631 (2008).
41. Kimura Y. N, et al. Inflammatory stimuli from macrophages and cancer cells synergistically promote tumour growth and angiogenesis. Cancer Sci 98, 2009-2018 (2007).
42. Colegio O. R, et al. Functional polarization of tumour-Associated macrophages by tumour-derived lactic acid. Nature (2014).
43. Tripathi C, et al. Macrophages are recruited to hypoxic tumour areas and acquire a Pro-Angiogenic M2-Polarized phenotype via hypoxic cancer cell derived cytokines Oncostatin M and Eotaxin. Oncotarget 5, 5350-5368 (2014).
44. Parker K, et al. HMGB1 enhances immune suppression by facilitating the differentiation and suppressive activity of myeloidderived suppressor cells. Cancer Res (2014).
45. Yan W, et al. High-mobility group box 1 activates caspase-1 and promotes hepatocellular carcinoma invasiveness and metastases. Hepatology 55, 1863-1875 (2012).
46. van Beijnum J. R, et al. Tumour angiogenesis is enforced by autocrine regulation of high-mobility group box 1. Oncogene 32, 363-374 (2013).
47. Taguchi A, et al. Blockade of RAGE-Amphoterin signalling suppresses tumour growth and metastases. Nature 405, 354-360 (2000).
48. He Y, et al. Tissue damage-Associated danger signals influence T-cell responses that promote the progression of preneoplasia to cancer. Cancer Res 73, 629-639 (2013).
49. Bald T, et al. Ultraviolet-radiation-induced inflammation promotes angiotropism and metastasis in melanoma. Nature 507, 109-113 (2014).
50. Liu Z, Falo L. D, Jr, & You Z. Knockdown of HMGB1 in tumour cells attenuates their ability to induce regulatory T cells and uncovers naturally acquired CD8 T cell-dependent antitumour immunity. J Immunol 187, 118-125 (2011).
51. Terai M, et al. Interleukin 6 mediates production of interleukin 10 in metastatic melanoma. Cancer Immunol Immunother 61, 145-155 (2012).
52. Kurte M, et al. A synthetic peptide homologous to functional domain of human IL-10 down-regulates expression of MHC class I and Transporter associated with Antigen Processing 1/2 in human melanoma cells. J Immunol 173, 1731-1737 (2004).
53. Carter N. A, Rosser E. C, & Mauri C. Interleukin-10 produced by B cells is crucial for the suppression of Th17/Th1 responses, induction of T regulatory type 1 cells and reduction of collagen-induced arthritis. Arthritis Res Ther 14, R32 (2012).
54. Carter N. A, et al. Mice lacking endogenous IL-10-producing regulatory B cells develop exacerbated disease and present with an increased frequency of Th1/Th17 but a decrease in regulatory T cells. J Immunol 186, 5569-5579 (2011).
55. Chen Q, Daniel V, Maher D. W, & Hersey P. Production of IL-10 by melanoma cells: examination of its role in immunosuppression mediated by melanoma. Int J Cancer 56, 755-760 (1994).
56. Mahipal A, et al. Tumour-derived interleukin-10 as a prognostic factor in stage III patients undergoing adjuvant treatment with an autologous melanoma cell vaccine. Cancer Immunol Immunother: CII 60, 1039-1045 (2011).
57. Zhao C. B, et al. Co-expression of RAGE and HMGB1 is associated with cancer progression and poor patient outcome of prostate cancer. Am J Cancer Res 4, 369-377 (2014).
58. Coffelt S. B, & Scandurro A. B. Tumours sound the alarmin(s). Cancer Res 68, 6482-6485 (2008).