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PMID: 19218341 Published · ppublish English Journal Article Research Support, N.I.H., Extramural

High-density gene expression analysis of tumor-associated macrophages from mouse mammary tumors.

The American journal of pathology ·Vol. 174 ·No. 3 ·2009-03-00 ·Pages 1048-64

Ojalvo LS, King W, Cox D, Pollard JW

Abstract

Clinical and experimental evidence indicates that tumor-associated macrophages (TAMs) promote malignant progression. In breast cancer, TAMs enhance tumor angiogenesis, tumor cell invasion, matrix remodeling, and immune suppression against the tumor. In this study, we examined late-stage mammary tumors from a transgenic mouse model of breast cancer. We used flow cytometry under conditions that minimized gene expression changes to isolate a rigorously defined TAM population previously shown to be associated with invasive carcinoma cells. The gene expression signature of this population was compared with a similar population derived from spleens of non-tumor-bearing mice using high-density oligonucleotide arrays. Using stringent selection criteria, transcript abundance of 460 genes was shown to be differentially regulated between the two populations. Bioinformatic analyses of known functions of these genes indicated that formerly ascribed TAM functions, including suppression of immune activation and matrix remodeling, as well as multiple mediators of tumor angiogenesis, were elevated in TAMs. Further bioinformatic analyses confirmed that a pure and valid TAM gene expression signature in mouse tumors could be used to assess expression of TAMs in human breast cancer. The data derived from these more physiologically relevant autochthonous tumors compared with previous studies in tumor xenografts suggest tactics by which TAMs may regulate tumor angiogenesis and thus provide a basis for exploring other transcriptional mediators of TAM trophic functions within the tumor microenvironment.

MeSH Terms
Animals Female Flow Cytometry Gene Expression Profiling Gene Expression Regulation, Neoplastic Humans Immunophenotyping Macrophages/pathology Mammary Neoplasms, Animal/genetics,pathology Mammary Neoplasms, Experimental/genetics Mice Mice, Transgenic Oligonucleotide Array Sequence Analysis Spleen/physiology
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Ojalvo Laureen S
Department of Developmental and Molecular Biology, Albert Einstein College of Medicine, 1300 Morris Park Avenue, Bronx, NY 10461, USA.
King William
Cox Dianne
Pollard Jeffrey W
References (72)
72 references, click to expand
  1. Tie2 identifies a hematopoietic lineage of proangiogenic monocytes required for tumor vessel formation and a mesenchymal population of pericyte progenitors.
    Cancer Cell. 2005 Sep;8(3):211-26 PMID: 16169466
  2. Tumor-associated macrophages press the angiogenic switch in breast cancer.
    Cancer Res. 2007 Jun 1;67(11):5064-6 PMID: 17545580
  3. Macrophages induce invasiveness of epithelial cancer cells via NF-kappa B and JNK.
    J Immunol. 2005 Jul 15;175(2):1197-205 PMID: 16002723
  4. The role of tumour-associated macrophages in tumour progression: implications for new anticancer therapies.
    J Pathol. 2002 Mar;196(3):254-65 PMID: 11857487
  5. IL-12 rapidly alters the functional profile of tumor-associated and tumor-infiltrating macrophages in vitro and in vivo.
    J Immunol. 2007 Feb 1;178(3):1357-62 PMID: 17237382
  6. SMAD4-deficient intestinal tumors recruit CCR1+ myeloid cells that promote invasion.
    Nat Genet. 2007 Apr;39(4):467-75 PMID: 17369830
  7. Cluster analysis and display of genome-wide expression patterns.
    Proc Natl Acad Sci U S A. 1998 Dec 8;95(25):14863-8 PMID: 9843981
  8. ONCOMINE: a cancer microarray database and integrated data-mining platform.
    Neoplasia. 2004 Jan-Feb;6(1):1-6 PMID: 15068665
  9. Macrophages express osteopontin during repair of myocardial necrosis.
    Am J Pathol. 1994 Dec;145(6):1450-62 PMID: 7992848
  10. Syk is required for monocyte/macrophage chemotaxis to CX3CL1 (Fractalkine).
    J Immunol. 2005 Sep 15;175(6):3737-45 PMID: 16148119
  11. Evidence for a role of osteopontin in macrophage infiltration in response to pathological stimuli in vivo.
    Am J Pathol. 1998 Feb;152(2):353-8 PMID: 9466560
  12. Osteopontin expression and distribution in human carcinomas.
    Am J Pathol. 1994 Sep;145(3):610-23 PMID: 8080043
  13. Colony-stimulating factor 1 promotes progression of mammary tumors to malignancy.
    J Exp Med. 2001 Mar 19;193(6):727-40 PMID: 11257139
  14. Systemic endocrine instigation of indolent tumor growth requires osteopontin.
    Cell. 2008 Jun 13;133(6):994-1005 PMID: 18555776
  15. Extracellular protease mRNAs are predominantly expressed in the stromal areas of microdissected mouse breast carcinomas.
    Carcinogenesis. 2005 Jul;26(7):1233-40 PMID: 15760918
  16. Characterisation and trophic functions of murine embryonic macrophages based upon the use of a Csf1r-EGFP transgene reporter.
    Dev Biol. 2007 Aug 1;308(1):232-46 PMID: 17597598
  17. A macrophage colony-stimulating factor receptor-green fluorescent protein transgene is expressed throughout the mononuclear phagocyte system of the mouse.
    Blood. 2003 Feb 1;101(3):1155-63 PMID: 12393599
  18. Abrogation of TGF beta signaling in mammary carcinomas recruits Gr-1+CD11b+ myeloid cells that promote metastasis.
    Cancer Cell. 2008 Jan;13(1):23-35 PMID: 18167337
  19. Macrophages promote collagen fibrillogenesis around terminal end buds of the developing mammary gland.
    Dev Dyn. 2006 Dec;235(12):3222-9 PMID: 17029292
  20. Macrophages in the embryo and beyond: much more than just giant phagocytes.
    Genesis. 2008 Sep;46(9):447-62 PMID: 18781633
  21. Exploration, normalization, and summaries of high density oligonucleotide array probe level data.
    Biostatistics. 2003 Apr;4(2):249-64 PMID: 12925520
  22. Subsets of myeloid-derived suppressor cells in tumor-bearing mice.
    J Immunol. 2008 Oct 15;181(8):5791-802 PMID: 18832739
  23. Circulating levels of colony-stimulating factor 1 as a prognostic indicator in 82 patients with epithelial ovarian cancer.
    Br J Cancer. 1994 Feb;69(2):342-6 PMID: 8297732
  24. Prediction of survival in follicular lymphoma based on molecular features of tumor-infiltrating immune cells.
    N Engl J Med. 2004 Nov 18;351(21):2159-69 PMID: 15548776
  25. Anti-colony-stimulating factor-1 antibody staining in primary breast adenocarcinomas correlates with marked inflammatory cell infiltrates and prognosis.
    J Natl Cancer Inst. 1994 Jan 19;86(2):120-6 PMID: 8271294
  26. Requirement of macrophages and eosinophils and their cytokines/chemokines for mammary gland development.
    Breast Cancer Res. 2002;4(4):155-64 PMID: 12100741
  27. Oncomine 3.0: genes, pathways, and networks in a collection of 18,000 cancer gene expression profiles.
    Neoplasia. 2007 Feb;9(2):166-80 PMID: 17356713
  28. Activated macrophages promote Wnt signalling through tumour necrosis factor-alpha in gastric tumour cells.
    EMBO J. 2008 Jun 18;27(12):1671-81 PMID: 18511911
  29. The detection and localization of monocyte chemoattractant protein-1 (MCP-1) in human ovarian cancer.
    J Clin Invest. 1995 May;95(5):2391-6 PMID: 7738202
  30. Molecular portraits of human breast tumours.
    Nature. 2000 Aug 17;406(6797):747-52 PMID: 10963602
  31. Macrophages: obligate partners for tumor cell migration, invasion, and metastasis.
    Cell. 2006 Jan 27;124(2):263-6 PMID: 16439202
  32. Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors.
    Cancer Res. 2007 Mar 15;67(6):2649-56 PMID: 17363585
  33. Mouse neutrophilic granulocytes express mRNA encoding the macrophage colony-stimulating factor receptor (CSF-1R) as well as many other macrophage-specific transcripts and can transdifferentiate into macrophages in vitro in response to CSF-1.
    J Leukoc Biol. 2007 Jul;82(1):111-23 PMID: 17438263
  34. Inflammation and cancer: breast cancer as a prototype.
    Breast. 2007 Dec;16 Suppl 2:S27-33 PMID: 17764938
  35. Macrophages promote the invasion of breast carcinoma cells via a colony-stimulating factor-1/epidermal growth factor paracrine loop.
    Cancer Res. 2005 Jun 15;65(12):5278-83 PMID: 15958574
  36. An amino-bisphosphonate targets MMP-9-expressing macrophages and angiogenesis to impair cervical carcinogenesis.
    J Clin Invest. 2004 Sep;114(5):623-33 PMID: 15343380
  37. Mesenchymal stem cells within tumour stroma promote breast cancer metastasis.
    Nature. 2007 Oct 4;449(7162):557-63 PMID: 17914389
  38. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche.
    Nature. 2005 Dec 8;438(7069):820-7 PMID: 16341007
  39. Osteopontin induces multiple changes in gene expression that reflect the six "hallmarks of cancer" in a model of breast cancer progression.
    Mol Carcinog. 2005 Aug;43(4):225-36 PMID: 15864800
  40. Distinct role of macrophages in different tumor microenvironments.
    Cancer Res. 2006 Jan 15;66(2):605-12 PMID: 16423985
  41. Significance of macrophage chemoattractant protein-1 in macrophage recruitment, angiogenesis, and survival in human breast cancer.
    Clin Cancer Res. 2000 Aug;6(8):3282-9 PMID: 10955814
  42. Progression to malignancy in the polyoma middle T oncoprotein mouse breast cancer model provides a reliable model for human diseases.
    Am J Pathol. 2003 Nov;163(5):2113-26 PMID: 14578209
  43. Syngeneic mouse mammary carcinoma cell lines: two closely related cell lines with divergent metastatic behavior.
    Clin Exp Metastasis. 2005;22(1):47-59 PMID: 16132578
  44. The role of osteopontin in tumor progression and metastasis in breast cancer.
    Cancer Epidemiol Biomarkers Prev. 2007 Jun;16(6):1087-97 PMID: 17548669
  45. Macrophages regulate the angiogenic switch in a mouse model of breast cancer.
    Cancer Res. 2006 Dec 1;66(23):11238-46 PMID: 17114237
  46. Macrophage lineage cells in inflammation: characterization by colony-stimulating factor-1 (CSF-1) receptor (c-Fms), ER-MP58, and ER-MP20 (Ly-6C) expression.
    Blood. 1998 Aug 15;92(4):1423-31 PMID: 9694732
  47. CSF-1 and its receptor in ovarian, endometrial and breast cancer.
    Ann Med. 1995 Feb;27(1):79-85 PMID: 7742005
  48. Structure and function of the spleen.
    Nat Rev Immunol. 2005 Aug;5(8):606-16 PMID: 16056254
  49. A distinct and unique transcriptional program expressed by tumor-associated macrophages (defective NF-kappaB and enhanced IRF-3/STAT1 activation).
    Blood. 2006 Mar 1;107(5):2112-22 PMID: 16269622
  50. Ovarian cancer cells polarize macrophages toward a tumor-associated phenotype.
    J Immunol. 2006 Apr 15;176(8):5023-32 PMID: 16585599
  51. Postnatal mammary gland development requires macrophages and eosinophils.
    Development. 2000 Jun;127(11):2269-82 PMID: 10804170
  52. Wnt 5a signaling is critical for macrophage-induced invasion of breast cancer cell lines.
    Proc Natl Acad Sci U S A. 2006 Apr 4;103(14):5454-9 PMID: 16569699
  53. Enhanced invasiveness of breast cancer cell lines upon co-cultivation with macrophages is due to TNF-alpha dependent up-regulation of matrix metalloproteases.
    Carcinogenesis. 2004 Aug;25(8):1543-9 PMID: 15044327
  54. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method.
    Methods. 2001 Dec;25(4):402-8 PMID: 11846609
  55. Significance analysis of microarrays applied to the ionizing radiation response.
    Proc Natl Acad Sci U S A. 2001 Apr 24;98(9):5116-21 PMID: 11309499
  56. Tumor-associated macrophages in breast cancer.
    J Mammary Gland Biol Neoplasia. 2002 Apr;7(2):177-89 PMID: 12463738
  57. Osteopontin expression in a group of lymph node negative breast cancer patients.
    Int J Cancer. 1998 Oct 23;79(5):502-8 PMID: 9761120
  58. Tumor angiogenesis and progression are enhanced by Sema4D produced by tumor-associated macrophages.
    J Exp Med. 2008 Jul 7;205(7):1673-85 PMID: 18559453
  59. The role of colony-stimulating factor 1 and its receptor in the etiopathogenesis of endometrial adenocarcinoma.
    Clin Cancer Res. 1995 Mar;1(3):313-25 PMID: 9815987
  60. Colony-stimulating factor-1 antisense treatment suppresses growth of human tumor xenografts in mice.
    Cancer Res. 2002 Sep 15;62(18):5317-24 PMID: 12235002
  61. Induction of mammary tumors by expression of polyomavirus middle T oncogene: a transgenic mouse model for metastatic disease.
    Mol Cell Biol. 1992 Mar;12(3):954-61 PMID: 1312220
  62. Macrophage receptors and immune recognition.
    Annu Rev Immunol. 2005;23:901-44 PMID: 15771589
  63. Vascular endothelial growth factor restores delayed tumor progression in tumors depleted of macrophages.
    Mol Oncol. 2007 Dec;1(3):288-302 PMID: 18509509
  64. Significant correlation of monocyte chemoattractant protein-1 expression with neovascularization and progression of breast carcinoma.
    Cancer. 2001 Sep 1;92(5):1085-91 PMID: 11571719
  65. A paracrine loop between tumor cells and macrophages is required for tumor cell migration in mammary tumors.
    Cancer Res. 2004 Oct 1;64(19):7022-9 PMID: 15466195
  66. Role of osteopontin in tumour progression.
    Br J Cancer. 2004 May 17;90(10):1877-81 PMID: 15138464
  67. Tumour-educated macrophages promote tumour progression and metastasis.
    Nat Rev Cancer. 2004 Jan;4(1):71-8 PMID: 14708027
  68. A gene-expression signature as a predictor of survival in breast cancer.
    N Engl J Med. 2002 Dec 19;347(25):1999-2009 PMID: 12490681
  69. Influence of lymphocytes on the presence and organization of dendritic cell subsets in the spleen.
    J Immunol. 1999 Nov 1;163(9):4894-900 PMID: 10528191
  70. Tumor-induced tolerance and immune suppression by myeloid derived suppressor cells.
    Immunol Rev. 2008 Apr;222:162-79 PMID: 18364001
  71. The macrophage growth factor CSF-1 in mammary gland development and tumor progression.
    J Mammary Gland Biol Neoplasia. 2002 Apr;7(2):147-62 PMID: 12465600
  72. "Re-educating" tumor-associated macrophages by targeting NF-kappaB.
    J Exp Med. 2008 Jun 9;205(6):1261-8 PMID: 18490490
Article Info
Journal
The American journal of pathology
Abbr.
Am J Pathol
ISSN
1525-2191
Published
2009-03-00
Epub
2009-00-13
Pages
1048-64
Language
English
Region
United States
NLM ID
0370502
PMCID
PMC2665764
Subset
IM
Grants
NCI NIH HHS · P01 CA100324 · United States
NCI NIH HHS · R01 CA131270 · United States
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