CSF1-ETS2-induced microRNA in myeloid cells promote metastatic tumor growth

Oncogene

Volumn 34, Issue 28, 2015, Pages 3651-3661

  Mathsyaraja, H ^a,b   Thies, K ^a,b   Taffany, D A ^a,b   Deighan, C ^c   Liu, T ^b   Yu, L ^b   Fernandez, S A ^b   Shapiro, C ^a,b   Otero, J ^a,b   Timmers, C ^b   Lustberg, M B ^a,b   Chalmers, J ^b,c   Leone, G ^a,b   Ostrowski, M C ^a,b  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c Ohio State University   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COLONY STIMULATING FACTOR 1; ETS2 PROTEIN, HUMAN; MICRORNA; MIRN142 MICRORNA, HUMAN; MIRN21 MICRORNA, HUMAN; MIRN223 MICRORNA, HUMAN; MIRN29 MICRORNA, HUMAN; TRANSCRIPTION FACTOR ETS 2;

ANIMAL; BREAST TUMOR; C57BL MOUSE; CELL PROLIFERATION; EXPERIMENTAL MELANOMA; FEMALE; GENETICS; HUMAN; MACROPHAGE; METABOLISM; MOUSE; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; SECONDARY; SIGNAL TRANSDUCTION; TUMOR CELL LINE; VASCULARIZATION;

ANIMALS; BREAST NEOPLASMS; CELL LINE, TUMOR; CELL PROLIFERATION; FEMALE; HUMANS; MACROPHAGE COLONY-STIMULATING FACTOR; MACROPHAGES; MELANOMA, EXPERIMENTAL; MICE; MICE, INBRED C57BL; MICRORNAS; NEOVASCULARIZATION, PATHOLOGIC; PROTO-ONCOGENE PROTEIN C-ETS-2; SIGNAL TRANSDUCTION;

EID: 84954027952     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2014.294     Document Type: Article

References (58)

1. Bröcker EB, Zwadlo G, Suter L, Brune M, Sorg C. Infiltration of primary and metastatic melanomas with macrophages of the 25F9-positive phenotype. Cancer Immunol Immunother 1987; 25: 81-86.
2. Leek RD, Harris AL. Tumor-associated macrophages in breast cancer. J Mammary Gland Biol Neoplasia 2002; 7: 177-189.
3. Jensen TO, Schmidt H, Møller HJ, Høyer M, Maniecki MB, Sjoegren P et al. Macrophage markers in serum and tumor have prognostic impact in American Joint Committee on Cancer stage I/II melanoma. J Clin Oncol 2009; 27: 3330-3337.
4. Qian BZ, Pollard JW. Macrophage diversity enhances tumor progression and metastasis. Cell 2010; 141: 39-51.
5. Chen Q, Zhang XH, Massague J. Macrophage binding to receptor VCAM-1 transmits survival signals in breast cancer cells that invade the lungs. Cancer Cell 2011; 20: 538-549.
6. Qian B, Deng Y, Im JH, Muschel RJ, Zou YLi J et al. A distinct macrophage population mediates metastatic breast cancer cell extravasation, establishment and growth. PLoS One 2009; 4: E6562.
7. Qian BZ, Li J, Zhang H, Kitamura T, Zhang J, Campion LR et al. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature 2011; 475: 222-225.
8. Yan HH, Pickup M, Pang Y, Gorska AE, Li Z, Chytil A et al. Gr-1+CD11b+ myeloid cells tip the balance of immune protection to tumor promotion in the premetastatic lung. Cancer Res 2010; 70: 6139-6149.
9. Wang T, Ge Y, Xiao M, Lopez-Coral A, Azuma R, Somasundaram R et al. Melanomaderived conditioned media efficiently induce the differentiation of monocytes to macrophages that display a highly invasive gene signature. Pigment Cell Melanoma Res 2012; 4: 493-505.
10. Chen P, Huang Y, Bong R, Ding Y, Song N, Wang X et al. Tumor-associated macrophages promote angiogenesis and melanoma growth via adrenomedullin in a paracrine and autocrine manner. Clin Cancer Res 2011; 17: 7230-7239.
11. Zaidi MR, Davis S, Noonan FP, Graff-Cherry C, Hawley TS, Walker RL et al. Interferon-? links ultraviolet radiation to melanomagenesis in mice. Nature 2011; 469: 548-553.
12. Esquela-Kerscher A, Slack FJ. Oncomirs-microRNAs with a role in cancer. Nat Rev Cancer 2006; 6: 259-269.
13. O'Connell RM, Rao DS, Chaudhuri AA, Baltimore D. Physiological and pathological roles for microRNAs in the immune system. Nat Rev Immunol 2010; 10: 111-122.
14. Liu G, Abraham E. MicroRNAs in immune response and macrophage polarization. Arterioscler Thromb Vasc Biol 2013; 33: 170-177.
15. Squadrito ML, Pucci F, Magri L, Moi D, Gilfillan GD, Ranghetti A et al. miR-511-3p modulates genetic programs of tumor-associated macrophages. Cell Rep 2012; 1: 141-154.
16. Zonari E, Pucci F, Saini M, Mazzieri R, Politi LS, Gentner B et al. A role for miR-155 in enabling tumor-infiltrating innate immune cells to mount effective anti-tumor responses. Blood 2013; 122: 243-252.
17. Zabuawala T, Taffany DA, Sharma SM, Merchant A, Adair B, Srinivasan R et al. An ets2-driven transcriptional program in tumor-associated macrophages promotes tumor metastasis. Cancer Res 2010; 70: 1323-1333.
18. Fowles LF, Martin ML, Nelsen L, Stacey KJ, Redd D, Clark YM et al. Persistent activation of mitogen-activated protein kinases p42 and p44 and ets-2 phosphorylation in response to colony-stimulating factor 1/c-fms signaling. Mol Cell Biol 1998; 18: 5148-5156.
19. Conway JG, McDonald B, Parham J, Keith B, Rusnak DW, Shaw E et al. Inhibition of colony-stimulating-factor-1 signaling in vivo with the orally bioavailable cFMS kinase inhibitor GW2580. Proc Natl Acad Sci USA 2005; 102: 16078-16083.
20. Clausen BE, Burkhardt C, Reith W, Renkawitz R, Forster I. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res 1999; 8: 265-277.
21. Rae F, Woods K, Sasmono T, Campanale N, Taylor D, Ovchinnikov DA et al. Characterisation and trophic functions of murine embryonic macrophages based upon the use of a Csf1r-EGFP transgene reporter. Dev Biol 2007; 308: 232-246.
22. Tagliani E, Shi C, Nancy P, Tay CS, Pamer EG, Erlebacher A. Coordinate regulation of tissue macrophage and dendritic cell population dynamics by CSF-1. J Exp Med 2011; 208: 1901-1916.
23. Mossadegh-Keller N, Sarrazin S, Kandalla PK, Espinosa L, Stanley ER, Nutt S et al. M-CSF instructs myeloid lineage fate in single haematopoietic stem cells. Nature 2013; 497: 239-243.
24. Yan LX, Huang XF, Shao Q, Huang MY, Deng L, Wu QL et al. MicroRNA miR-21 overexpression in human breast cancer is associated with advanced clinical stage, lymph node metastasis and patient poor prognosis. RNA 2008; 14: 2348-2360.
25. Gebeshuber CA, Zatloukal K, Martinez J. miR-29a suppresses tristetraprolin, which is a regulator of epithelial polarity and metastasis. EMBO Rep 2009; 10: 400-405.
26. Gao D, Mittal V. The role of bone-marrow-derived cells in tumor growth, metastasis initiation and progression. Trends Mol Med 2009; 15: 333-343.
27. Gabrilovich DI, Ostrand-Rosenberg S, Bronte V. Coordinated regulation of myeloid cells by tumours. Nat Rev Immunol 2012; 22: 253-268.
28. Strauss-Ayali D, Conrad SM, Mosser DM. Monocyte subpopulations and their differentiation patterns during infection. J Leukoc Biol 2007; 82: 244-252.
29. Sica A, Bronte V. Altered macrophage differentiation and immune dysfunction in tumor development. J Clin Invest 2007; 117: 1155-1166.
30. De Palma M, Venneri MA, Galli R, Sergi Sergi L, Politi LS, Sampaolesi M et al. Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors. Cancer Cell 2005; 8: 211-226.
31. Lu TX, Hartner J, Lim EJ, Fabry V, Mingler MK, Cole ET et al. MicroRNA-21 limits in vivo immune response-mediated activation of the IL-12/IFN-gamma pathway, Th1 polarization, and the severity of delayed-type hypersensitivity. J Immunol 2011; 187: 3362-3373.
32. Ma F, Xu S, Liu X, Zhang Q, Xu X, Liu M et al. The microRNA miR-29 controls innate and adaptive immune responses to intracellular bacterial infection by targeting interferon-gamma. Nat Immunol 2011; 12: 861-869.
33. Sheedy FJ, Palsson-McDermott E, Hennessy EJ, Martin C, O'Leary JJ, Ruan Q et al. Negative regulation of TLR4 via targeting of the proinflammatory tumor suppressor PDCD4 by the microRNA miR-21. Nat Immunol 2010; 11: 141-147.
34. Sica A, Mantovani A. Macrophage plasticity and polarization: In vivo veritas. J Clin Invest 2012; 122: 787-795.
35. Brain O, Owens BM, Pichulik T, Allan P, Khatamzas E, Leslie A et al. The intracellular sensor NOD2 induces microRNA-29 expression in human dendritic cells to limit IL-23 release. Immunity 2013; 39: 521-536.
36. Qi JH, Ebrahem Q, Moore N, Murphy G, Claesson-Welsh L, Bond M et al. A novel function for tissue inhibitor of metalloproteinases-3 (TIMP3): Inhibition of angiogenesis by blockage of VEGF binding to VEGF receptor-2. Nat Med 2003; 9: 407-415.
37. Gabriely G, Wurdinger T, Kesari S, Esau CC, Burchard J, Linsley PS et al. MicroRNA promotes glioma invasion by targeting matrix metalloproteinase regulators. Mol Cell Biol 2008; 28: 5369-5380.
38. Marneros AG, Olsen BR. The role of collagen-derived proteolytic fragments in angiogenesis. Matrix Biol 2001; 20: 337-345.
39. Lamagna C, Aurrand-Lions M, Imhof BA. Dual role of macrophages in tumor growth and angiogenesis. J Leukoc Biol 2006; 80: 705-713.
40. Cho HJ, Jung JI, Lim do Y, Kwon GT, Her S, Park JH et al. Bone marrow-derived, alternatively activated macrophages enhance solid tumor growth and lung metastasis of mammary carcinoma cells in a Balb/C mouse orthotopic model. Breast Cancer Res 2012; 14: R81.
41. Fabbri M, Paone A, Calore F, Galli R, Gaudio E, Santhanam R et al. MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc Natl Acad Sci USA 2012; 109: E2110-E2116.
42. Yang M, Chen J, Su F, Yu B, Su F, Lin L et al. Microvesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells. Mol Cancer 2011; 10: 117.
43. Si ML, Zhu S, Wu H, Lu Z, Wu F, Mo YY. miR-21-mediated tumor growth. Oncogene 2007; 26: 2799-2803.
44. Croce CM. Causes and consequences of microRNA dysregulation in cancer. Nat Rev Genet 2009; 10: 704-714.
45. Chou J, Lin JH, Brenot A, Kim JW, Provot S, Werb Z. GATA3 suppresses metastasis and modulates the tumour microenvironment by regulating microRNA-29b expression. Nat Cell Biol 2013; 15: 201-213.
46. Kumar MS, Pester RE, Chen CY, Lane K, Chin C, Lu J et al. Dicer1 functions as a haploinsufficient tumor suppressor. Genes Dev 2009; 23: 2700-2704.
47. DeNardo DG, Brennan DJ, Rexhepaj E, Ruffell B, Shiao SL, Madden SF et al. Leukocyte complexity predicts breast cancer survival and functionally regulates response to chemotherapy. Cancer Discov 2011; 1: 54-67.
48. Priceman SJ, Sung JL, Shaposhnik Z, Burton JB, Torres-Collado AX, Moughon DL et al. Targeting distinct tumor-infiltrating myeloid cells by inhibiting CSF-1 receptor: Combating tumor evasion of antiangiogenic therapy. Blood 2010; 115: 1461-1471.
49. Pyonteck SM, Akkari L, Schuhmacher AJ, Bowman RL, Sevenich L, Quail DF et al. CSF-1R inhibition alters macrophage polarization and blocks glioma progression. Nat Med 2013; 19: 1264-1272.
50. Mok S, Koya RC, Tsui C, Xu J, Robert L, Wu L et al. Inhibition of CSF1 receptor improves the anti-tumor efficacy of adoptive cell transfer immunotherapy. Cancer Res 2014; 74: 153-161.
51. Wei G, Guo J, Doseff AI, Kusewitt DF, Man AK, Oshima RG et al. Activated Ets2 is required for persistent inflammatory responses in the motheaten viable model. J Immunol 2004; 173: 1374-1379.
52. Yamamoto H, Flannery ML, Kupriyanov S, Pearce J, McKercher SR, Henkel GW et al. Defective trophoblast function in mice with a targeted mutation of Ets2. Genes Dev 1998; 12: 1315-1326.
53. Pei XF, Noble MS, Davoli MA, Rosfjord E, Tilli MT, Furth PA et al. Explant-cell culture of primary mammary tumors from MMTV-c-Myc transgenic mice. In Vitro Cell Dev Biol Anim 2004; 40: 14-21.
54. Dunham LJ, Stewart HL. A survey of transplantable and transmissible animal tumors. J Nat Cancer Inst 1953; 13: 1299-1377.
55. Fidler IJ. Biological behavior of malignant melanoma cells correlated to their survival in vivo. Cancer Res 1975; 35: 218-224.
56. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T et al. Fiji: An open-source platform for biological-image analysis. Nat Methods 2012; 9: 676-682.
57. Hu R, Sharma SM, Bronisz A, Srinivasan R, Sankar U, Ostrowski MC. Eos, MITF, and PU.1 recruit corepressors to osteoclast-specific genes in committed myeloid progenitors. Mol Cell Biol 2007; 27: 4018-4027.
58. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25: 402-408.