Low infiltration of tumor-associated macrophages in high c-Myb-expressing breast tumors

. 2019 Aug 12 ; 9 (1) : 11634. [epub] 20190812

Jazyk angličtina Země Anglie, Velká Británie Médium electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid31406165
Odkazy

PubMed 31406165
PubMed Central PMC6690941
DOI 10.1038/s41598-019-48051-1
PII: 10.1038/s41598-019-48051-1
Knihovny.cz E-zdroje

Tumor-associated macrophages (TAMs) are prominent components of tumor stroma that promotes tumorigenesis. Many soluble factors participate in the deleterious cross-talk between TAMs and transformed cells; however mechanisms how tumors orchestrate their production remain relatively unexplored. c-Myb is a transcription factor recently described as a negative regulator of a specific immune signature involved in breast cancer (BC) metastasis. Here we studied whether c-Myb expression is associated with an increased presence of TAMs in human breast tumors. Tumors with high frequency of c-Myb-positive cells have lower density of CD68-positive macrophages. The negative association is reflected by inverse correlation between MYB and CD68/CD163 markers at the mRNA levels in evaluated cohorts of BC patients from public databases, which was found also within the molecular subtypes. In addition, we identified potential MYB-regulated TAMs recruiting factors that in combination with MYB and CD163 provided a valuable clinical multigene predictor for BC relapse. We propose that identified transcription program running in tumor cells with high MYB expression and preventing macrophage accumulation may open new venues towards TAMs targeting and BC therapy.

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Yang L, Zhang Y. Tumor-associated macrophages: from basic research to clinical application. J Hematol Oncol. 2017;10:58. doi: 10.1186/s13045-017-0430-2. PubMed DOI PMC

Kim J, Bae JS. Tumor-Associated Macrophages and Neutrophils in Tumor Microenvironment. Mediators Inflamm. 2016;2016:6058147. PubMed PMC

Mantovani A, Sozzani S, Locati M, Allavena P, Sica A. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol. 2002;23:549–55. doi: 10.1016/S1471-4906(02)02302-5. PubMed DOI

Valković T, et al. Correlation between vascular endothelial growth factor, angiogenesis, and tumor-associated macrophages in invasive ductal breast. Virchows Arch. 2002;440:583–8. doi: 10.1007/s004280100458. PubMed DOI

Li W, et al. The association between expressions of Ras and CD68 in the angiogenesis of breast cancers. Cancer Cell Int. 2015;15:17. doi: 10.1186/s12935-015-0169-1. PubMed DOI PMC

Bolat F, et al. Microvessel density, VEGF expression, and tumor-associated macrophages in breast tumors: correlations with prognostic parameters. J Exp Clin Cancer Res. 2006;25:365–72. PubMed

Ruffell B, Coussens LM. Macrophages and Therapeutic Resistance in Cancer. Cancer Cell. 2015;27:462–72. doi: 10.1016/j.ccell.2015.02.015. PubMed DOI PMC

De Palma M, Lewis CE. Cancer: Macrophages limit chemotherapy. Nature. 2011;472:303–4. doi: 10.1038/472303a. PubMed DOI

Yuan ZY, Luo RZ, Peng RJ, Wang SS, Xue C. High infiltration of tumor-associated macrophages in triple-negative breast cancer is associated with a higher risk of distant metastasis. Onco Targets Ther. 2014;7:1475–80. doi: 10.2147/OTT.S61838. PubMed DOI PMC

Campbell MJ, et al. Proliferating macrophages associated with high grade, hormone receptor negative breast cancer and poor clinical outcome. Breast Cancer Res Treat. 2011;128:703–711. doi: 10.1007/s10549-010-1154-y. PubMed DOI PMC

Zeisberger SM, et al. Clodronate-liposome-mediated depletion of tumour-associated macrophages: a new and highly effective antiangiogenic therapy approach. Br J Cancer. 2006;95:272–81. doi: 10.1038/sj.bjc.6603240. PubMed DOI PMC

Rogers TL, Holen I. Tumour macrophages as potential targets of bisphosphonates. J Transl Med. 2011;9:177. doi: 10.1186/1479-5876-9-177. PubMed DOI PMC

Giraudo E, Inoue M, Hanahan D. An amino-bisphosphonate targets MMP-9-expressing macrophages and angiogenesis to impair cervical carcinogenesis. J Clin Invest. 2004;114:623–33. doi: 10.1172/JCI200422087. PubMed DOI PMC

Tsagozis P, Eriksson F, Pisa P. Zoledronic acid modulates antitumoral responses of prostate cancer-tumor associated macrophages. Cancer Immunol Immunother. 2008;57:1451–9. doi: 10.1007/s00262-008-0482-9. PubMed DOI PMC

Borsig L, Wolf MJ, Roblek M, Lorentzen A, Heikenwalder M. Inflammatory chemokines and metastasis-tracing the accessory. Oncogene. 2014;33:3217–24. doi: 10.1038/onc.2013.272. PubMed DOI

Ramsay RG, Gonda TJ. MYB function in normal and cancer cells. Nat Rev Cancer. 2008;8:523–34. doi: 10.1038/nrc2439. PubMed DOI

Drabsch Y, Robert RG, Gonda TJ. MYB suppresses differentiation and apoptosis of human breast cancer cells. Breast Cancer Res. 2010;12:R55. doi: 10.1186/bcr2614. PubMed DOI PMC

Miao RY, et al. MYB is essential for mammary tumorigenesis. Cancer Res. 2011;71:7029–37. doi: 10.1158/0008-5472.CAN-11-1015. PubMed DOI

Thorner AR, Parker JS, Hoadley KA, Perou CM. Potential tumor suppressor role for the c-Myb oncogene in luminal breast cancer. PLoS One. 2010;5:e13073. doi: 10.1371/journal.pone.0013073. PubMed DOI PMC

Nicolau M, Levine AJ, Carlsson G. Topology based data analysis identifies a subgroup of breast cancers with a unique mutational profile and excellent survival. Proc Natl Acad Sci USA. 2011;108:7265–70. doi: 10.1073/pnas.1102826108. PubMed DOI PMC

Hugo HJ, et al. Direct repression of MYB by ZEB1 suppresses proliferation and epithelial gene expression during epithelial-to-mesenchymal transition of breast cancer cells. Breast Cancer Res. 2013;15:R113. doi: 10.1186/bcr3580. PubMed DOI PMC

Liu LY, et al. A supervised network analysis on gene expression profiles of breast tumors predicts a 41-gene prognostic signature of the transcription factor MYB across molecular subtypes. Comput Math Methods Med. 2014;2014:813067. PubMed PMC

Knopfová L, et al. Transcription factor c-Myb inhibits breast cancer lung metastasis by suppression of tumor cell seeding. Oncogene. 2018;37:1020–1030. doi: 10.1038/onc.2017.392. PubMed DOI PMC

Fang WB, et al. Targeted gene silencing of CCL2 inhibits triple negative breast cancer progression by blocking cancer stem cell renewal and M2 macrophage recruitment. Oncotarget. 2016;7:49349–49367. PubMed PMC

Kitamura T, et al. CCL2-induced chemokine cascade promotes breast cancer metastasis by enhancing retention of metastasis-associated macrophages. J Exp Med. 2015;212:1043–59. doi: 10.1084/jem.20141836. PubMed DOI PMC

Qian BZ, et al. CCL2 recruits inflammatory monocytes to facilitate breast-tumour metastasis. Nature. 2011;475:222–5. doi: 10.1038/nature10138. PubMed DOI PMC

Ueno T, et al. Significance of macrophage chemoattractant protein-1 in macrophage recruitment, angiogenesis, and survival in human breast cancer. Clin Cancer Res. 2000;6:3282–9. PubMed

Yao M, Yu E, Staggs V, Fan F, Cheng N. Elevated expression of chemokine C-C ligand 2 in stroma is associated with recurrent basal-like breast cancers. Mod Pathol. 2016;29:810–23. doi: 10.1038/modpathol.2016.78. PubMed DOI

Medrek C, Pontén F, Jirström 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. doi: 10.1186/1471-2407-12-306. PubMed DOI PMC

Glück S, et al. TP53 genomics predict higher clinical and pathologic tumor response in operable early-stage breast cancer treated with docetaxel-capecitabine ± trastuzumab. Breast Cancer Res Treat. 2012;132:781–91. doi: 10.1007/s10549-011-1412-7. PubMed DOI

Itoh M, et al. Estrogen receptor (ER) mRNA expression and molecular subtype distribution in ER-negative/progesterone receptor-positive breast cancers. Breast Cancer Res Treat. 2014;143:403–9. doi: 10.1007/s10549-013-2763-z. PubMed DOI

Chanmee T, Ontong P, Konno K, Itano N. Tumor-associated macrophages as major players in the tumor microenvironment. Cancers (Basel) 2014;6:1670–90. doi: 10.3390/cancers6031670. PubMed DOI PMC

Casazza A, et al. Impeding macrophage entry into hypoxic tumor areas by Sema3A/Nrp1 signaling blockade inhibits angiogenesis and restores antitumor immunity. Cancer Cell. 2013;24:695–709. doi: 10.1016/j.ccr.2013.11.007. PubMed DOI

Singh S, et al. Initiative action of tumor-associated macrophage during tumor metastasis. Biochim Open. 2017;4:8–18. doi: 10.1016/j.biopen.2016.11.002. PubMed DOI PMC

Hollmén M, et al. G-CSF regulates macrophage phenotype and associates with poor overall survival in human triple-negative breast cancer. Oncoimmunology. 2015;5:e1115177. doi: 10.1080/2162402X.2015.1115177. PubMed DOI PMC

Argyle D, Kitamura T. Targeting Macrophage-Recruiting Chemokines as a Novel Therapeutic Strategy to Prevent the Progression of Solid Tumors. Front Immunol. 2018;9:2629. doi: 10.3389/fimmu.2018.02629. PubMed DOI PMC

Aguirre-Gamboa R, et al. SurvExpress: an online biomarker validation tool and database for cancer gene expression data using survival analysis. PLoS One. 2013;8:e74250. doi: 10.1371/journal.pone.0074250. PubMed DOI PMC

Györffy B, et al. An online survival analysis tool to rapidly assess the effect of 22,277 genes on breast cancer prognosis using microarray data of 1,809 patients. Breast Cancer Res Treat. 2010;123:725–31. doi: 10.1007/s10549-009-0674-9. PubMed DOI

Shabo I, Stål O, Olsson H, Doré S, Svanvik J. Breast cancer expression of CD163, a macrophage scavenger receptor, is related to early distant recurrence and reduced patient survival. Int J Cancer. 2008;123:780–6. doi: 10.1002/ijc.23527. PubMed DOI

Tichý M, et al. Overexpression of c-Myb is associated with suppression of distant metastases in colorectal carcinoma. Tumour Biol. 2016;37:10723–9. doi: 10.1007/s13277-016-4956-7. PubMed DOI

Tichý M, et al. High c-Myb Expression Associates with Good Prognosis in Colorectal Carcinoma. J Cancer. 2019;10:1393–7. doi: 10.7150/jca.29530. PubMed DOI PMC

Knopfová L, et al. c-Myb regulates matrix metalloproteinases 1/9, and cathepsin D: implications for matrix-dependent breast cancer cell invasion and metastasis. Mol Cancer. 2012;11:15. doi: 10.1186/1476-4598-11-15. PubMed DOI PMC

Landskron G, De la Fuente M, Thuwajit P, Thuwajit C, Hermoso MA. Chronic inflammation and cytokines in the tumor microenvironment. J Immunol Res. 2014;2014(():149185. PubMed PMC

Condeelis J, Pollard JW. Macrophages: obligate partners for tumor cell migration, invasion, and metastasis. Cell. 2006;124:263–6. doi: 10.1016/j.cell.2006.01.007. PubMed DOI

Zhao X, et al. Prognostic significance of tumor-associated macrophages in breast cancer: a meta-analysis of the literature. Oncotarget. 2017;8:30576–30586. PubMed PMC

Noy R, Pollard JW. Tumor-associated macrophages: from mechanisms to therapy. Immunity. 2014;41:49–61. doi: 10.1016/j.immuni.2014.06.010. PubMed DOI PMC

Steele RJ, Eremin O, Brown M, Hawkins RA. Oestrogen receptor concentration and macrophage infiltration in human breast cancer. Eur J Surg Oncol. 1986;12:273–6. PubMed

Gonda TJ, Leo P, Ramsay RG. Estrogen and MYB in breast cancer: potential for new therapies. Expert Opin Biol Ther. 2008;8:713–7. doi: 10.1517/14712598.8.6.713. PubMed DOI

Sousa S, et al. Human breast cancer cells educate macrophages toward the M2 activation status. Breast Cancer Res. 2015;17:101. doi: 10.1186/s13058-015-0621-0. PubMed DOI PMC

Tiainen S, et al. High numbers of macrophages, especially M2-like (CD163-positive), correlate with hyaluronan accumulation and poor outcome in breast cancer. Histopathology. 2015;66:873–83. doi: 10.1111/his.12607. PubMed DOI

Aras S, Zaidi MR. TAMeless traitors: macrophages in cancer progression and metastasis. Br J Cancer. 2017;117:1583–1591. doi: 10.1038/bjc.2017.356. PubMed DOI PMC

Linde N, et al. Vascular endothelial growth factor-induced skin carcinogenesis depends on recruitment and alternative activation of macrophages. J Pathol. 2012;227:17–28. doi: 10.1002/path.3989. PubMed DOI

Barleon B, et al. Migration of human monocytes in response to vascular endothelial growth factor (VEGF) is mediated via the VEGF receptor flt-1. Blood. 1996;87:3336–43. PubMed

Bonapace L, et al. Cessation of CCL2 inhibition accelerates breast cancer metastasis by promoting angiogenesis. Nature. 2014;515:130–3. doi: 10.1038/nature13862. PubMed DOI

Tymoszuk P, et al. In situ proliferation contributes to accumulation of tumor-associated macrophages in spontaneous mammary tumors. Eur J Immunol. 2014;44:2247–62. doi: 10.1002/eji.201344304. PubMed DOI

Wallerius M, et al. Guidance Molecule SEMA3A Restricts Tumor Growth by Differentially Regulating the Proliferation of Tumor-Associated Macrophages. Cancer Res. 2016;76:3166–78. doi: 10.1158/0008-5472.CAN-15-2596. PubMed DOI

Boulakirba S, et al. IL-34 and CSF-1 display an equivalent macrophage differentiation ability but a different polarization potential. Sci Rep. 2018;8:256. doi: 10.1038/s41598-017-18433-4. PubMed DOI PMC

Scholl SM, et al. Anti-colony-stimulating factor-1 antibody staining in primary breast adenocarcinomas correlates with marked inflammatory cell infiltrates and prognosis. J Natl Cancer Inst. 1994;86:120–6. doi: 10.1093/jnci/86.2.120. PubMed DOI

Aharinejad S, et al. Elevated CSF1 serum concentration predicts poor overall survival in women with early breast cancer. Endocr Relat Cancer. 2013;20:777–83. doi: 10.1530/ERC-13-0198. PubMed DOI

Richardsen E, Uglehus RD, Johnsen SH, Busund LT. Macrophage-colony stimulating factor (CSF1) predicts breast cancer progression and mortality. Anticancer Res. 2015;35:865–74. PubMed

Kluger HM, et al. Macrophage colony-stimulating factor-1 receptor expression is associated with poor outcome in breast cancer by large cohort tissue microarray analysis. Clin Cancer Res. 2004;10:173–7. doi: 10.1158/1078-0432.CCR-0699-3. PubMed DOI

Zins K, Heller G, Mayerhofer M, Schreiber M, Abraham D. Differential prognostic impact of interleukin-34 mRNA expression and infiltrating immune cell composition in intrinsic breast cancer subtypes. Oncotarget. 2018;9:23126–23148. doi: 10.18632/oncotarget.25226. PubMed DOI PMC

Swierczak A, et al. The promotion of breast cancer metastasis caused by inhibition of CSF-1R/CSF-1 signaling is blocked by targeting the G-CSF receptor. Cancer. Immunol Res. 2014;2:765–76. PubMed

Laoui D, Van Overmeire E, De Baetselier P, Van Ginderachter JA, Raes G. Functional Relationship between Tumor-Associated Macrophages and Macrophage Colony-Stimulating Factor as Contributors to Cancer Progression. Front Immunol. 2014;5:489. doi: 10.3389/fimmu.2014.00489. PubMed DOI PMC

Beck AH, et al. The macrophage colony-stimulating factor 1 response signature in breast carcinoma. Clin Cancer Res. 2009;15:778–87. doi: 10.1158/1078-0432.CCR-08-1283. PubMed DOI PMC

Lin EY, Nguyen AV, Russell RG, Pollard JW. Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy. J Exp Med. 2001;193:727–40. doi: 10.1084/jem.193.6.727. PubMed DOI PMC

Qian B, et al. A distinct macrophage population mediates metastatic breast cancer cell extravasation, establishment and growth. PLoS One. 2009;4:e6562. doi: 10.1371/journal.pone.0006562. PubMed DOI PMC

Aharinejad S, et al. Colony-stimulating factor-1 blockade by antisense oligonucleotides and small interfering RNAs suppresses growth of human mammary tumor xenografts in mice. Cancer Res. 2004;64:5378–84. doi: 10.1158/0008-5472.CAN-04-0961. PubMed DOI

Ries CH, et al. Targeting tumor-associated macrophages with anti-CSF-1R antibody reveals a strategy for cancer therapy. Cancer Cell. 2014;25:846–59. doi: 10.1016/j.ccr.2014.05.016. PubMed DOI

Strachan DC, et al. CSF1R inhibition delays cervical and mammary tumor growth in murine models by attenuating the turnover of tumor-associated macrophages and enhancing infiltration by CD8+ T cells. Oncoimmunology. 2013;2:e26968. doi: 10.4161/onci.26968. PubMed DOI PMC

Linde N, et al. Macrophages orchestrate breast cancer early dissemination and metastasis. Nat Commun. 2018;9:21. doi: 10.1038/s41467-017-02481-5. PubMed DOI PMC

Qiu SQ, et al. Tumor-associated macrophages in breast cancer: Innocent bystander or important player? Cancer Treat Rev. 2018;70:178–189. doi: 10.1016/j.ctrv.2018.08.010. PubMed DOI

Minn AJ, et al. Genes that mediate breast cancer metastasis to lung. Nature. 2005;436:518–24. doi: 10.1038/nature03799. PubMed DOI PMC

McShane LM, et al. REporting recommendations for tumor MARKer prognostic studies (REMARK) Breast Cancer Res Treat. 2006;100:229–35. doi: 10.1007/s10549-006-9242-8. PubMed DOI

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