Integrated miRNA and mRNA profiling of tumor-educated macrophages identifies prognostic subgroups in estrogen receptor-positive breast cancer

Molecular Oncology

Volumn 9, Issue 1, 2015, Pages 155-166

  Bleckmann, Annalen ^a   Leha, Andreas ^a   Artmann, Stephan ^a   Menck, Kerstin ^a   Salinas Riester, Gabriela ^a   Binder, Claudia ^a   Pukrop, Tobias ^a   Beissbarth, Tim ^a   Klemm, Florian ^a  

^a UNIVERSITY MEDICAL CENTER GÖTTINGEN   (Germany)

Author keywords

Breast cancer; MiRNA; Tumor associated macrophages

Indexed keywords

CD14 ANTIGEN; CHLORDANE; MICRORNA; MICRORNA 125A 5P; MICRORNA 128; MICRORNA 128A 9.1; MICRORNA 135A; MICRORNA 181D; MICRORNA 210; MICRORNA 296 5P; MICRORNA 30A; MICRORNA 486 5P; MICRORNA 493; MICRORNA 548C 5P; MICRORNA 578; MICRORNA 767 3P; MICRORNA 769 3P; MICRORNA 941; TAMOXIFEN; UNCLASSIFIED DRUG; ESTROGEN RECEPTOR; MESSENGER RNA;

ARTICLE; ASSESSMENT OF HUMANS; BREAST CANCER CELL LINE; BRIER SCORE; CANCER PROGNOSIS; CANCER SURVIVAL; COCULTURE; DISEASE FREE SURVIVAL; ESTROGEN RECEPTOR POSITIVE BREAST CANCER; GENE EXPRESSION; GENE EXPRESSION PROFILING; HUMAN; HUMAN CELL; HUMAN TISSUE; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SURVIVAL PREDICTION; TUMOR ASSOCIATED LEUKOCYTE; TUMOR EDUCATED MACROPHAGE; BIOSYNTHESIS; BREAST TUMOR; FEMALE; MACROPHAGE; MCF 7 CELL LINE; METABOLISM; MORTALITY; PATHOLOGY; SURVIVAL RATE;

BREAST NEOPLASMS; COCULTURE TECHNIQUES; DISEASE-FREE SURVIVAL; FEMALE; GENE EXPRESSION PROFILING; HUMANS; MACROPHAGES; MCF-7 CELLS; MICRORNAS; RECEPTORS, ESTROGEN; RNA, MESSENGER; SURVIVAL RATE;

EID: 84920445650     PISSN: 15747891     EISSN: 18780261     Source Type: Journal    
DOI: 10.1016/j.molonc.2014.07.023     Document Type: Article

References (51)

1. Allinen M., Beroukhim R., Cai L., Brennan C., Lahti-Domenici J., Huang H., Porter D., Hu M., Chin L., Richardson A., Schnitt S., Sellers W.R., Polyak K. Molecular characterization of the tumor microenvironment in breast cancer. Cancer Cell 2004, 6:17-32. 10.1016/j.ccr.2004.06.010.
2. Andersen P.K., Gill R.D. Cox's regression model for counting processes: a large sample study. Ann. Stat. 1982, 10:1100-1120. 10.1214/aos/1176345976.
3. Arranz E.E., Vara J.A., Gamez-Pozo A., Zamora P. Gene signatures in breast cancer: current and future uses. Transl. Oncol. 2012, 5:398-403.
4. Artmann S., Jung K., Bleckmann A., Beissbarth T. Detection of simultaneous group effects in microRNA expression and related target gene sets. PLoS One 2012, 7:e38365. 10.1371/journal.pone.0038365.
5. Barrett T., Edgar R. Gene expression omnibus: microarray data storage, submission, retrieval, and analysis. Methods Enzym. 2006, 411:352-369. 10.1016/S0076-6879(06)11019-8.
6. Benjamini Y., Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J.R. Statist. Soc. Ser. B (Methodological) 1995, 57:289-300. 10.2307/2346101.
7. Bezman N.A., Chakraborty T., Bender T., Lanier L.L. miR-150 regulates the development of NK and iNKT cells. J.Exp. Med. 2011, 208:2717-2731. 10.1084/jem.20111386.
8. Binder H., Schumacher M. Incorporating pathway information into boosting estimation of high-dimensional risk prediction models. BMC Bioinform. 2009, 10:18. 10.1186/1471-2105-10-18.
9. Brier G.W. Verification of forecasts expressed in terms of probability. Mon. Weather Rev. 1950, 78(1-3). 10.1175/1520-0493(1950)078<0001:VOFEIT>2.0.CO;2.
10. Brock G., Pihur V., Datta S., Datta S. clValid, an R package for cluster validation. J.Stat. Softw. 2011, 25:1-22. Brock Al March 2008.
11. Buffa F.M., Camps C., Winchester L., Snell C.E., Gee H.E., Sheldon H., Taylor M., Harris A.L., Ragoussis J. microRNA-associated progression pathways and potential therapeutic targets identified by integrated mRNA and microRNA expression profiling in breast Cancer. Cancer Res. 2011, 71:5635-5645. 10.1158/0008-5472.CAN-11-0489.
12. Camps C., Buffa F.M., Colella S., Moore J., Sotiriou C., Sheldon H., Harris A.L., Gleadle J.M., Ragoussis J. hsa-miR-210 is induced by hypoxia and is an independent prognostic factor in breast cancer. Clin. Cancer Res. 2008, 14:1340-1348. 10.1158/1078-0432.CCR-07-1755.
13. Cuzick J., Sestak I., Baum M., Buzdar A., Howell A., Dowsett M., Forbes J.F. Effect of anastrozole and tamoxifen as adjuvant treatment for early-stage breast cancer: 10-year analysis of the ATAC trial. Lancet Oncol. 2010, 11:1135-1141. 10.1016/S1470-2045(10)70257-6.
14. Du T., Zamore P.D. microPrimer: the biogenesis and function of microRNA. Development 2005, 132:4645-4652. 10.1242/dev.02070.
15. Durinck S., Moreau Y., Kasprzyk A., Davis S., De Moor B., Brazma A., Huber W. BioMart and Bioconductor: a powerful link between biological databases and microarray data analysis. Bioinformatics 2005, 21:3439-3440. 10.1093/bioinformatics/bti525.
16. Eiro N., Pidal I., Fernandez-Garcia B., Junquera S., Lamelas M.L., del Casar J.M., Gonzalez L.O., Lopez-Muniz A., Vizoso F.J. Impact of CD68/(CD3+CD20) ratio at the invasive front of primary tumors on distant metastasis development in breast cancer. PLoS One 2012, 7:e52796. 10.1371/journal.pone.0052796.
17. Esserman L.J., Moore D.H., Tsing P.J., Chu P.W., Yau C., Ozanne E., Chung R.E., Tandon V.J., Park J.W., Baehner F.L., Kreps S., Tutt A.N.J., Gillett C.E., Benz C.C. Biologic markers determine both the risk and the timing of recurrence in breast cancer. Breast Cancer Res. Treat. 2011, 129:607-616. 10.1007/s10549-011-1564-5.
18. Finak G., Bertos N., Pepin F., Sadekova S., Souleimanova M., Zhao H., Chen H., Omeroglu G., Meterissian S., Omeroglu A., Hallett M., Park M. Stromal gene expression predicts clinical outcome in breast cancer. Nat. Med. 2008, 14:518-527. 10.1038/nm1764.
19. Graff J.W., Dickson A.M., Clay G., McCaffrey A.P., Wilson M.E. Identifying functional microRNAs in macrophages with polarized phenotypes. J.Biol. Chem. 2012, 287:21816-21825. 10.1074/jbc.M111.327031.
20. Griffiths-Jones S., Saini H.K., van Dongen S., Enright A.J. miRBase: tools for microRNA genomics. Nucleic Acids Res. 2008, 36:D154-D158. 10.1093/nar/gkm952.
21. Guo H., Ingolia N.T., Weissman J.S., Bartel D.P. Mammalian microRNAs predominantly act to decrease target mRNA levels. Nature 2010, 466:835-840. 10.1038/nature09267.
22. Hagemann T., Wilson J., Kulbe H., Li N.F., Leinster D.A., Charles K., Klemm F., Pukrop T., Binder C., Balkwill F.R. Macrophages induce invasiveness of epithelial cancer cells via NF-κB and JNK. J.Immunol. 2005, 175:1197-1205.
23. He M., Xu Z., Ding T., Kuang D.M., Zheng L. MicroRNA-155 regulates inflammatory cytokine production in tumor-associated macrophages via targeting C/EBPbeta. Cell Mol. Immunol. 2009, 6:343-352. 10.1038/cmi.2009.45.
24. Hu H.Y., He L., Fominykh K., Yan Z., Guo S., Zhang X., Taylor M.S., Tang L., Li J., Liu J., Wang W., Yu H., Khaitovich P. Evolution of the human-specific microRNA miR-941. Nat. Commun. 2012, 3:1145. 10.1038/ncomms2146.
25. Laoui D., Movahedi K., Van Overmeire E., Van den Bossche J., Schouppe E., Mommer C., Nikolaou A., Morias Y., De Baetselier P., Van Ginderachter J.A. Tumor-associated macrophages in breast cancer: distinct subsets, distinct functions. Int. J. Dev. Biol. 2011, 55:861-867. 10.1387/ijdb.113371dl.
26. Leek R.D., Lewis C.E., Whitehouse R., Greenall M., Clarke J., Harris A.L. Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma. Cancer Res. 1996, 56:4625-4629.
27. Lyng M.B., Laenkholm A.V., Sokilde R., Gravgaard K.H., Litman T., Ditzel H.J. Global microRNA expression profiling of high-risk ER+ breast cancers from patients receiving adjuvant tamoxifen mono-therapy: a DBCG study. PLoS One 2012, 7:e36170. 10.1371/journal.pone.0036170.
28. Majewski I.J., Ritchie M.E., Phipson B., Corbin J., Pakusch M., Ebert A., Busslinger M., Koseki H., Hu Y., Smyth G.K., Alexander W.S., Hilton D.J., Blewitt M.E. Opposing roles of polycomb repressive complexes in hematopoietic stem and progenitor cells. Blood 2010, 116:731-739. 10.1182/blood-2009-12-260760.
29. Marot G., Mayer C.D. Sequential analysis for microarray data based on sensitivity and meta-analysis. Stat. Appl. Genet. Mol. Biol. 2009, 8. Article 3. 10.2202/1544-6115.1368.
30. Medrek C., Ponten F., Jirstrom K., Leandersson K. The presence of tumor associated macrophages in tumor stroma as a prognostic marker for breast cancer patients. BMC Cancer 2012, 12:306. 10.1186/1471-2407-12-306.
31. Nicoloso M.S., Spizzo R., Shimizu M., Rossi S., Calin G.A. MicroRNAs-the micro steering wheel of tumour metastases. Nat. Rev. Cancer 2009, 9:293-302. 10.1038/nrc2619.
32. Ojalvo L.S., Whittaker C.A., Condeelis J.S., Pollard J.W. Gene expression analysis of macrophages that facilitate tumor invasion supports a role for Wnt-signaling in mediating their activity in primary mammary tumors. J.Immunol. 2010, 184:702-712. 10.4049/jimmunol.0902360.
33. Parker J.S., Mullins M., Cheang M.C., Leung S., Voduc D., Vickery T., Davies S., Fauron C., He X., Hu Z., Quackenbush J.F., Stijleman I.J., Palazzo J., Marron J.S., Nobel A.B., Mardis E., Nielsen T.O., Ellis M.J., Perou C.M., Bernard P.S. Supervised risk predictor of breast cancer based on intrinsic subtypes. J.Clin. Oncol. 2009, 27:1160-1167. 10.1200/JCO.2008.18.1370.
34. Perou C.M., Sorlie T., Eisen M.B., van de Rijn M., Jeffrey S.S., Rees C.A., Pollack J.R., Ross D.T., Johnsen H., Akslen L.A., Fluge O., Pergamenschikov A., Williams C., Zhu S.X., Lonning P.E., Borresen-Dale A.L., Brown P.O., Botstein D. Molecular portraits of human breast tumours. Nature 2000, 406:747-752. 10.1038/35021093.
35. Pihur V., Datta S. RankAggreg, an R package for weighted rank aggregation. BMC Bioinform. 2009, 10:62. 10.1186/1471-2105-10-62.
36. Pukrop T., Klemm F., Hagemann T., Gradl D., Schulz M., Siemes S., Trümper L., Binder C. Wnt 5a signaling is critical for macrophage-induced invasion of breast cancer cell lines. Proc. Natl. Acad. Sci.U. S. A. 2006, 103:5454-5459. 10.1073/pnas.0509703103.
37. Qian B.Z., Pollard J.W. Macrophage diversity enhances tumor progression and metastasis. Cell 2010, 141:39-51. 10.1016/j.cell.2010.03.014.
38. Quail D.F., Joyce J.A. Microenvironmental regulation of tumor progression and metastasis. Nat. Med. 2013, 19:1423-1437. 10.1038/nm.3394.
39. R Development Core Team R: A Language and Environment for Statistical Computing 2013, R Foundation for Statistical Computing, Vienna, Austria.
40. Rothe F., Ignatiadis M., Chaboteaux C., Haibe-Kains B., Kheddoumi N., Majjaj S., Badran B., Fayyad-Kazan H., Desmedt C., Harris A.L., Piccart M., Sotiriou C. Global microRNA expression profiling identifies MiR-210 associated with tumor proliferation, invasion and poor clinical outcome in breast cancer. PLoS One 2011, 6:e20980. 10.1371/journal.pone.0020980.
41. Singer C.F., Gschwantler-Kaulich D., Fink-Retter A., Haas C., Hudelist G., Czerwenka K., Kubista E. Differential gene expression profile in breast cancer-derived stromal fibroblasts. Breast Cancer Res. Treat. 2008, 110:273-281. 10.1007/s10549-007-9725-2.
42. Smid M., Wang Y., Zhang Y., Sieuwerts A.M., Yu J., Klijn J.G., Foekens J.A., Martens J.W. Subtypes of breast cancer show preferential site of relapse. Cancer Res. 2008, 68:3108-3114. 10.1158/0008-5472.CAN-07-5644.
43. Sorlie T., Perou C.M., Tibshirani R., Aas T., Geisler S., Johnsen H., Hastie T., Eisen M.B., van de Rijn M., Jeffrey S.S., Thorsen T., Quist H., Matese J.C., Brown P.O., Botstein D., Lonning P.E., Borresen-Dale A.L. Gene expression patterns of breast carcinomas distinguish tumor subclasses with clinical implications. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:10869-10874. 10.1073/pnas.191367098.
44. Squadrito M.L., Etzrodt M., De Palma M., Pittet M.J. MicroRNA-mediated control of macrophages and its implications for cancer. Trends Immunol. 2013, 34:350-359. 10.1016/j.it.2013.02.003.
45. Squadrito M.L., Pucci F., Magri L., Moi D., Gilfillan G.D., Ranghetti A., Casazza A., Mazzone M., Lyle R., Naldini L., De Palma M. miR-511-3p modulates genetic programs of tumor-associated macrophages. Cell Rep. 2012, 1:141-154. 10.1016/j.celrep.2011.12.005.
46. Stouffer S.A. The American Soldier, Studies in Social Psychology in World War II 1949, Princeton University Press, Princeton.
47. Tian W., Chen J., He H., Deng Y. MicroRNAs and drug resistance of breast cancer: basic evidence and clinical applications. Clin. Transl. Oncol. 2013, 15:335-342. 10.1007/s12094-012-0929-5.
48. Volinia S., Galasso M., Sana M.E., Wise T.F., Palatini J., Huebner K., Croce C.M. Breast cancer signatures for invasiveness and prognosis defined by deep sequencing of microRNA. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:3024-3029. 10.1073/pnas.1200010109.
49. Wiel M.A.van de, Berkhof J., Wieringen W.N.van Testing the prediction error difference between 2 predictors. Biostatistics 2009, 10:550-560. 10.1093/biostatistics/kxp011.
50. Yang M., Chen J., Su F., Yu B., Lin L., Liu Y., Huang J.D., Song E. Microvesicles secreted by macrophages shuttle invasion-potentiating microRNAs into breast cancer cells. Mol. Cancer 2011, 10:117. 10.1186/1476-4598-10-117.
51. Zabuawala T., Taffany D.A., Sharma S.M., Merchant A., Adair B., Srinivasan R., Rosol T.J., Fernandez S., Huang K., Leone G., Ostrowski M.C. An ets2-driven transcriptional program in tumor-associated macrophages promotes tumor metastasis. Cancer Res. 2010, 70:1323-1333. 10.1158/0008-5472.CAN-09-1474.