Mesenchymal transition and dissemination of cancer cells is driven by myeloid-derived suppressor cells infiltrating the primary tumor

PLoS Biology

Volumn 9, Issue 9, 2011, Pages

  Toh, Benjamin ^a   Wang, Xiaojie ^a   Keeble, Jo ^a   Sim, Wen Jing ^b   Khoo, Karen ^a   Wong, Wing Cheong ^c   Kato, Masashi ^d   Prevost Blondel, Armelle ^e   Thiery, Jean Paul ^b,f   Abastado, Jean Pierre ^a  

^a AGENCY FOR SCIENCE   (Singapore)

^b INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Singapore)

^c BIOINFORMATICS INSTITUTE   (Singapore)

^d CHUBU UNIVERSITY   (Japan)

^e INSTITUT COCHIN   (France)

^f NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

Author keywords

[No Author keywords available]

Indexed keywords

CXCL1 CHEMOKINE; CXCL2 CHEMOKINE; EPIDERMAL GROWTH FACTOR; EPITHELIAL DERIVED NEUTROPHIL ACTIVATING FACTOR 78; MACROPHAGE INFLAMMATORY PROTEIN 3BETA; SCATTER FACTOR; TRANSFORMING GROWTH FACTOR BETA; CHEMOKINE; CHEMOKINE RECEPTOR CXCR2; DOPACHROME ISOMERASE; ISOMERASE; MICROPHTHALMIA ASSOCIATED TRANSCRIPTION FACTOR; MITF PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MARROW CELL; CANCER CELL; CANCER GROWTH; CELL ASSAY; CELL INFILTRATION; CELL MOTILITY; CELL PROLIFERATION; CONTROLLED STUDY; DISEASE MODEL; EPITHELIAL MESENCHYMAL TRANSITION; IN VITRO STUDY; INFLAMMATION; METASTASIS POTENTIAL; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PHENOTYPE; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SKIN METASTASIS; SUPPRESSOR CELL; UVEA MELANOMA; VISCERAL METASTASIS; ANIMAL; CELL MOTION; EXPERIMENTAL MELANOMA; GENE EXPRESSION PROFILING; GENETICS; GRANULOCYTE; LUNG; LYMPH NODE; METABOLISM; METASTASIS; PATHOLOGY; REAL TIME POLYMERASE CHAIN REACTION; SKIN TUMOR; TRANSGENIC MOUSE; TUMOR CELL CULTURE; UVEA TUMOR;

MURINAE;

ANIMALS; CELL MOVEMENT; CELL PROLIFERATION; CHEMOKINES; EPITHELIAL-MESENCHYMAL TRANSITION; GENE EXPRESSION PROFILING; GRANULOCYTES; INTRAMOLECULAR OXIDOREDUCTASES; LUNG; LYMPH NODES; MELANOMA, EXPERIMENTAL; MICE; MICE, TRANSGENIC; MICROPHTHALMIA-ASSOCIATED TRANSCRIPTION FACTOR; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, INTERLEUKIN-8B; SKIN NEOPLASMS; TUMOR CELLS, CULTURED; UVEAL NEOPLASMS;

EID: 80053336355     PISSN: 15449173     EISSN: 15457885     Source Type: Journal    
DOI: 10.1371/journal.pbio.1001162     Document Type: Article

References (72)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, et al. (2008) Cancer statistics, 2008. CA Cancer J Clin 58: 71-96.
2. Nguyen D. X, Bos P. D, Massague J, (2009) Metastasis: from dissemination to organ-specific colonization. Nat Rev Cancer 9: 274-284.
3. Fearon E. R, Vogelstein B, (1990) A genetic model for colorectal tumorigenesis. Cell 61: 759-767.
4. Bernards R, Weinberg R. A, (2002) A progression puzzle. Nature 418: 823.
5. Eyles J, Puaux A. L, Wang X, Toh B, Prakash C, et al. (2010) Tumor cells disseminate early, but immunosurveillance limits metastatic outgrowth, in a mouse model of melanoma. J Clin Invest 120: 2030-2039.
6. Husemann Y, Geigl J. B, Schubert F, Musiani P, Meyer M, et al. (2008) Systemic spread is an early step in breast cancer. Cancer Cell 13: 58-68.
7. Balkwill F, Mantovani A, (2001) Inflammation and cancer: back to Virchow? Lancet 357: 539-545.
8. Cordon-Cardo C, Prives C, (1999) At the crossroads of inflammation and tumorigenesis. J Exp Med 190: 1367-1370.
9. Grivennikov S. I, Greten F. R, Karin M, (2010) Immunity, inflammation, and cancer. Cell 140: 883-899.
10. Mantovani A, (2010) Molecular pathways linking inflammation and cancer. Curr Mol Med 10: 369-373.
11. DeNardo D. G, Andreu P, Coussens L. M, (2010) Interactions between lymphocytes and myeloid cells regulate pro- versus anti-tumor immunity. Cancer Metastasis Rev 29: 309-316.
12. Movahedi K, Laoui D, Gysemans C, Baeten M, Stange G, et al. (2010) Different tumor microenvironments contain functionally distinct subsets of macrophages derived from Ly6C(high) monocytes. Cancer Res 70: 5728-5739.
13. Bronte V, (2009) Myeloid-derived suppressor cells in inflammation: uncovering cell subsets with enhanced immunosuppressive functions. Eur J Immunol 39: 2670-2672.
14. Gabrilovich D. I, Nagaraj S, (2009) Myeloid-derived suppressor cells as regulators of the immune system. Nat Rev Immunol 9: 162-174.
15. Ostrand-Rosenberg S, Sinha P, (2009) Myeloid-derived suppressor cells: linking inflammation and cancer. J Immunol 182: 4499-4506.
16. Ribechini E, Greifenberg V, Sandwick S, Lutz M. B, (2010) Subsets, expansion and activation of myeloid-derived suppressor cells. Med Microbiol Immunol 199: 273-281.
17. Peranzoni E, Zilio S, Marigo I, Dolcetti L, Zanovello P, et al. (2010) Myeloid-derived suppressor cell heterogeneity and subset definition. Curr Opin Immunol 22: 238-244.
18. Movahedi K, Guilliams M, Van den Bossche J, Van den Bergh R, Gysemans C, et al. (2008) Identification of discrete tumor-induced myeloid-derived suppressor cell subpopulations with distinct T cell-suppressive activity. Blood 111: 4233-4244.
19. Youn J. I, Nagaraj S, Collazo M, Gabrilovich D. I, (2008) Subsets of myeloid-derived suppressor cells in tumor-bearing mice. J Immunol 181: 5791-5802.
20. Yang L, Edwards C. M, Mundy G. R, (2010) Gr-1+CD11b+ myeloid-derived suppressor cells: formidable partners in tumor metastasis. J Bone Miner Res 25: 1701-1706.
21. Murdoch C, Muthana M, Coffelt S. B, Lewis C. E, (2008) The role of myeloid cells in the promotion of tumour angiogenesis. Nat Rev Cancer 8: 618-631.
22. Ostrand-Rosenberg S, (2010) Myeloid-derived suppressor cells: more mechanisms for inhibiting antitumor immunity. Cancer Immunol Immunother 59: 1593-1600.
23. Kato M, Takahashi M, Akhand A. A, Liu W, Dai Y, et al. (1998) Transgenic mouse model for skin malignant melanoma. Oncogene 17: 1885-1888.
24. Eskelin S, Pyrhonen S, Summanen P, Hahka-Kemppinen M, Kivela T, (2000) Tumor doubling times in metastatic malignant melanoma of the uvea: tumor progression before and after treatment. Ophthalmology 107: 1443-1449.
25. Alla V, Engelmann D, Niemetz A, Pahnke J, Schmidt A, et al. (2010) E2F1 in melanoma progression and metastasis. J Natl Cancer Inst 102: 127-133.
26. Thiery J. P, Acloque H, Huang R. Y, Nieto M. A, (2009) Epithelial-mesenchymal transitions in development and disease. Cell 139: 871-890.
27. Landsberg J, Gaffal E, Cron M, Kohlmeyer J, Renn M, et al. (2010) Autochthonous primary and metastatic melanomas in Hgf-Cdk4 R24C mice evade T-cell-mediated immune surveillance. Pigment Cell Melanoma Res 23: 649-660.
28. Bronkhorst I. H, Ly L. V, Jordanova E. S, Vrolijk J, Versluis M, et al. (2011) Detection of M2-macrophages in uveal melanoma and relation with survival. Invest Ophthalmol Vis Sci 52: 643-650.
29. Nagendra S, Schlueter A. J, (2004) Absence of cross-reactivity between murine Ly-6C and Ly-6G. Cytometry A 58: 195-200.
30. Narang V, Wong S. Y, Leong S. R, Abastado J. P, Gouaillard A, Comparing mathematical models of cell adhesion in tumors; 2011; 2nd International Conference on Computational Systems- Biology and Bioinformatics. Singapore.
31. Ferreira S. C Jr, Martins M. L, Vilela M. J, (2002) Reaction-diffusion model for the growth of avascular tumor. Phys Rev E Stat Nonlin Soft Matter Phys 65: 021907.
32. Mallet D. G, De Pillis L. G, (2006) A cellular automata model of tumor-immune system interactions. J Theor Biol 239: 334-350.
33. Billottet C, Tuefferd M, Gentien D, Rapinat A, Thiery J. P, et al. (2008) Modulation of several waves of gene expression during FGF-1 induced epithelial-mesenchymal transition of carcinoma cells. J Cell Biochem 104: 826-839.
34. Gavrilovic J, Moens G, Thiery J. P, Jouanneau J, (1990) Expression of transfected transforming growth factor alpha induces a motile fibroblast-like phenotype with extracellular matrix-degrading potential in a rat bladder carcinoma cell line. Cell Regul 1: 1003-1014.
35. Jouanneau J, Gavrilovic J, Caruelle D, Jaye M, Moens G, et al. (1991) Secreted or nonsecreted forms of acidic fibroblast growth factor produced by transfected epithelial cells influence cell morphology, motility, and invasive potential. Proc Natl Acad Sci U S A 88: 2893-2897.
36. Thiery J. P, (2002) Epithelial-mesenchymal transitions in tumour progression. Nat Rev Cancer 2: 442-454.
37. Helfman D. M, Kim E. J, Lukanidin E, Grigorian M, (2005) The metastasis associated protein S100A4: role in tumour progression and metastasis. Br J Cancer 92: 1955-1958.
38. Grum-Schwensen B, Klingelhofer J, Berg C. H, El-Naaman C, Grigorian M, et al. (2005) Suppression of tumor development and metastasis formation in mice lacking the S100A4(mts1) gene. Cancer Res 65: 3772-3780.
39. Boye K, Maelandsmo G. M, (2010) S100A4 and metastasis: a small actor playing many roles. Am J Pathol 176: 528-535.
40. Klein C. A, (2009) Parallel progression of primary tumours and metastases. Nat Rev Cancer 9: 302-312.
41. Melani C, Chiodoni C, Forni G, Colombo M. P, (2003) Myeloid cell expansion elicited by the progression of spontaneous mammary carcinomas in c-erbB-2 transgenic BALB/c mice suppresses immune reactivity. Blood 102: 2138-2145.
42. Eash K. J, Greenbaum A. M, Gopalan P. K, Link D. C, (2010) CXCR2 and CXCR4 antagonistically regulate neutrophil trafficking from murine bone marrow. J Clin Invest 120: 2423-2431.
43. Chintakuntlawar A. V, Chodosh J, (2009) Chemokine CXCL1/KC and its receptor CXCR2 are responsible for neutrophil chemotaxis in adenoviral keratitis. J Interferon Cytokine Res 29: 657-666.
44. Dhawan P, Richmond A, (2002) Role of CXCL1 in tumorigenesis of melanoma. J Leukoc Biol 72: 9-18.
45. Gutman M, Singh R. K, Xie K, Bucana C. D, Fidler I. J, (1995) Regulation of interleukin-8 expression in human melanoma cells by the organ environment. Cancer Res 55: 2470-2475.
46. Yang J, Weinberg R. A, (2008) Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Dev Cell 14: 818-829.
47. Gupta P. B, Kuperwasser C, Brunet J. P, Ramaswamy S, Kuo W. L, et al. (2005) The melanocyte differentiation program predisposes to metastasis after neoplastic transformation. Nat Genet 37: 1047-1054.
48. Moody S. E, Perez D, Pan T. C, Sarkisian C. J, Portocarrero C. P, et al. (2005) The transcriptional repressor Snail promotes mammary tumor recurrence. Cancer Cell 8: 197-209.
49. Keirsebilck A, Bonne S, Bruyneel E, Vermassen P, Lukanidin E, et al. (1998) E-cadherin and metastasin (mts-1/S100A4) expression levels are inversely regulated in two tumor cell families. Cancer Res 58: 4587-4591.
50. Andersen K, Nesland J. M, Holm R, Florenes V. A, Fodstad O, et al. (2004) Expression of S100A4 combined with reduced E-cadherin expression predicts patient outcome in malignant melanoma. Mod Pathol 17: 990-997.
51. Norton L, (2005) Conceptual and practical implications of breast tissue geometry: toward a more effective, less toxic therapy. Oncologist 10: 370-381.
52. Yang L, Huang J, Ren X, Gorska A. E, Chytil A, et al. (2008) Abrogation of TGF beta signaling in mammary carcinomas recruits Gr-1+CD11b+ myeloid cells that promote metastasis. Cancer Cell 13: 23-35.
53. Kitamura T, Kometani K, Hashida H, Matsunaga A, Miyoshi H, et al. (2007) SMAD4-deficient intestinal tumors recruit CCR1+ myeloid cells that promote invasion. Nat Genet 39: 467-475.
54. Bierie B, Moses H. L, (2010) Transforming growth factor beta (TGF-beta) and inflammation in cancer. Cytokine Growth Factor Rev 21: 49-59.
55. Cahill D. P, Kinzler K. W, Vogelstein B, Lengauer C, (1999) Genetic instability and darwinian selection in tumours. Trends Cell Biol 9: M57-M60.
56. Chaffer C. L, Weinberg R. A, (2011) A perspective on cancer cell metastasis. Science 331: 1559-1564.
57. Ledford H, (2011) Cancer theory faces doubts. Nature 472: 273.
58. Qian B. Z, Pollard J. W, (2010) Macrophage diversity enhances tumor progression and metastasis. Cell 141: 39-51.
59. Lin E. Y, Nguyen A. V, Russell R. G, Pollard J. W, (2001) Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy. J Exp Med 193: 727-740.
60. Robinson B. D, Sica G. L, Liu Y. F, Rohan T. E, Gertler F. B, et al. (2009) Tumor microenvironment of metastasis in human breast carcinoma: a potential prognostic marker linked to hematogenous dissemination. Clin Cancer Res 15: 2433-2441.
61. Doedens A. L, Stockmann C, Rubinstein M. P, Liao D, Zhang N, et al. (2010) Macrophage expression of hypoxia-inducible factor-1{alpha} suppresses T-cell function and promotes tumor progression. Cancer Res.
62. Greifenberg V, Ribechini E, Rossner S, Lutz M. B, (2009) Myeloid-derived suppressor cell activation by combined LPS and IFN-gamma treatment impairs DC development. Eur J Immunol 39: 2865-2876.
63. Sinha P, Clements V. K, Bunt S. K, Albelda S. M, Ostrand-Rosenberg S, (2007) Cross-talk between myeloid-derived suppressor cells and macrophages subverts tumor immunity toward a type 2 response. J Immunol 179: 977-983.
64. Marigo I, Bosio E, Solito S, Mesa C, Fernandez A, et al. (2010) Tumor-induced tolerance and immune suppression depend on the C/EBPbeta transcription factor. Immunity 32: 790-802.
65. Hanson E. M, Clements V. K, Sinha P, Ilkovitch D, Ostrand-Rosenberg S, (2009) Myeloid-derived suppressor cells down-regulate L-selectin expression on CD4+ and CD8+ T cells. J Immunol 183: 937-944.
66. Corzo C. A, Cotter M. J, Cheng P, Cheng F, Kusmartsev S, et al. (2009) Mechanism regulating reactive oxygen species in tumor-induced myeloid-derived suppressor cells. J Immunol 182: 5693-5701.
67. Rosenberg S. A, Yang J. C, Restifo N. P, (2004) Cancer immunotherapy: moving beyond current vaccines. Nat Med 10: 909-915.
68. Yang L, DeBusk L. M, Fukuda K, Fingleton B, Green-Jarvis B, et al. (2004) Expansion of myeloid immune suppressor Gr+CD11b+ cells in tumor-bearing host directly promotes tumor angiogenesis. Cancer Cell 6: 409-421.
69. Lengagne R, Graff-Dubois S, Garcette M, Renia L, Kato M, et al. (2008) Distinct role for CD8 T cells toward cutaneous tumors and visceral metastases. J Immunol 180: 130-137.
70. Faust N, Varas F, Kelly L. M, Heck S, Graf T, (2000) Insertion of enhanced green fluorescent protein into the lysozyme gene creates mice with green fluorescent granulocytes and macrophages. Blood 96: 719-726.
71. Lopez A. F, Strath M, Sanderson C. J, (1984) Differentiation antigens on mouse eosinophils and neutrophils identified by monoclonal antibodies. Br J Haematol 57: 489-494.
72. Abramoff M. D, Magelhaes P. J, Ram S. J, (2004) Image processing with ImageJ. Biophotonics International 11: 36-42.