Phenotyping of tumor-associated macrophages in colorectal cancer: Impact on single cell invasion (tumor budding) and clinicopathological outcome

References

• Hanahan D, Weinberg RA. Hallmarks of cancer: the next generation. Cell 2011; 144:646-74; PMID:21376230; http://dx.doi.org/10.1016/j.cell.2011.02.013
   PubMed Web of Science ®Google Scholar
• Raggi C, Mousa HS, Correnti M, Sica A, Invernizzi P. Cancer stem cells and tumor-associated macrophages: a roadmap for multitargeting strategies. Oncogene 2015; 35:671-82; PMID:25961921; http://dx.doi.org/10.1038/onc.2015.132
   PubMed Web of Science ®Google Scholar
• Heusinkveld M, van der Burg SH. Identification and manipulation of tumor associated macrophages in human cancers. J Transl Med 2011; 9:216; PMID:22176642; http://dx.doi.org/10.1186/1479-5876-9-216
   PubMed Web of Science ®Google Scholar
• Lau SK, Chu PG, Weiss LM. CD163: a specific marker of macrophages in paraffin-embedded tissue samples. Am J Clin Pathol 2004; 122:794-801; PMID:15491976; http://dx.doi.org/10.1309/QHD6YFN81KQ-XUUH6
   PubMed Web of Science ®Google Scholar
• Biswas SK, Mantovani A. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat Immunol 2010; 11:889-96; PMID:20856220; http://dx.doi.org/10.1038/ni.1937
   PubMed Web of Science ®Google Scholar
• Hao NB, Lu MH, Fan YH, Cao YL, Zhang ZR, Yang SM. Macrophages in tumor microenvironments and the progression of tumors. Clin Dev Immunol 2012; 2012:948098; PMID:22778768; http://dx.doi.org/10.1155/2012/948098
   PubMed Web of Science ®Google Scholar
• Calon A, Lonardo E, Berenguer-Llergo A, Espinet E, Hernando-Momblona X, Iglesias M, Sevillano M, Palomo-Ponce S, Tauriello DV, Byrom D et al. Stromal gene expression defines poor-prognosis subtypes in colorectal cancer. Nat Genet 2015; 47:320-9; PMID:25706628; http://dx.doi.org/10.1038/ng.3225
   PubMed Web of Science ®Google Scholar
• Zlobec I, Lugli A. Epithelial mesenchymal transition and tumor budding in aggressive colorectal cancer: tumor budding as oncotarget. Oncotarget 2010; 1:651-61; PMID:21317460; http://dx.doi.org/10.18632/oncotarget.199
   PubMed Web of Science ®Google Scholar
• Bronsert P, Enderle-Ammour K, Bader M, Timme S, Kuehs M, Csanadi A, Kayser G, Kohler I, Bausch D, Hoeppner J et al. Cancer cell invasion and EMT marker expression: a three-dimensional study of the human cancer-host interface. J Pathol 2014; 234:410-22; PMID:25081610; http://dx.doi.org/10.1002/path.4416
   PubMed Web of Science ®Google Scholar
• Zavadil J, Bottinger EP. TGF-beta and epithelial-to-mesenchymal transitions. Oncogene 2005; 24:5764-74; PMID:16123809; http://dx.doi.org/10.1038/sj.onc.1208927
   PubMed Web of Science ®Google Scholar
• Isella C, Terrasi A, Bellomo SE, Petti C, Galatola G, Muratore A, Mellano A, Senetta R, Cassenti A, Sonetto C et al. Stromal contribution to the colorectal cancer transcriptome. Nat Genet 2015; 47:312-9; PMID:25706627; http://dx.doi.org/10.1038/ng.3224
   PubMed Web of Science ®Google Scholar
• Lugli A, Karamitopoulou E, Zlobec I. Tumour budding: a promising parameter in colorectal cancer. Br J Cancer 2012; 106:1713-7; PMID:22531633; http://dx.doi.org/10.1038/bjc.2012.127
   PubMed Web of Science ®Google Scholar
• Mitrovic B, Schaeffer DF, Riddell RH, Kirsch R. Tumor budding in colorectal carcinoma: time to take notice. Mod Pathol 2012; 25:1315-25; PMID:22790014; http://dx.doi.org/10.1038/modpathol.2012.94
   PubMed Web of Science ®Google Scholar
• Calon A, Espinet E, Palomo-Ponce S, Tauriello DV, Iglesias M, Cespedes MV, Sevillano M, Nadal C, Jung P, Zhang XH et al. Dependency of colorectal cancer on a TGF-beta-driven program in stromal cells for metastasis initiation. Cancer Cell 2012; 22:571-84; PMID:23153532; http://dx.doi.org/10.1016/j.ccr.2012.08.013
   PubMed Web of Science ®Google Scholar
• Putoczki TL, Thiem S, Loving A, Busuttil RA, Wilson NJ, Ziegler PK, Nguyen PM, Preaudet A, Farid R, Edwards KM et al. Interleukin-11 is the dominant IL-6 family cytokine during gastrointestinal tumorigenesis and can be targeted therapeutically. Cancer Cell 2013; 24:257-71; PMID:23948300; http://dx.doi.org/10.1016/j.ccr.2013.06.017
   PubMed Web of Science ®Google Scholar
• Faber TJ, Japink D, Leers MP, Sosef MN, von Meyenfeldt MF, Nap M. Activated macrophages containing tumor marker in colon carcinoma: immunohistochemical proof of a concept. Tumour Biol 2012; 33:435-41; PMID:22134871; http://dx.doi.org/10.1007/s13277-011-0269-z
   PubMed Web of Science ®Google Scholar
• Chao MP, Weissman IL, Majeti R. The CD47-SIRPalpha pathway in cancer immune evasion and potential therapeutic implications. Curr Opin Immunol 2012; 24:225-32; PMID:22310103; http://dx.doi.org/10.1016/j.coi.2012.01.010
   PubMed Web of Science ®Google Scholar
• Majeti R, Chao MP, Alizadeh AA, Pang WW, Jaiswal S, Gibbs KD, Jr., van Rooijen N, Weissman IL. CD47 is an adverse prognostic factor and therapeutic antibody target on human acute myeloid leukemia stem cells. Cell 2009; 138:286-99; PMID:19632179; http://dx.doi.org/10.1016/j.cell.2009.05.045
   PubMed Web of Science ®Google Scholar
• Willingham SB, Volkmer JP, Gentles AJ, Sahoo D, Dalerba P, Mitra SS, Wang J, Contreras-Trujillo H, Martin R, Cohen JD et al. The CD47-signal regulatory protein alpha (SIRPa) interaction is a therapeutic target for human solid tumors. Proc Natl Acad Sci U S A 2012; 109:6662-7; PMID:22451913; http://dx.doi.org/10.1073/pnas.1121623109
   PubMed Web of Science ®Google Scholar
• Zhang Y, Sime W, Juhas M, Sjolander A. Crosstalk between colon cancer cells and macrophages via inflammatory mediators and CD47 promotes tumour cell migration. Eur J Cancer 2013; 49:3320-34; PMID:23810249; http://dx.doi.org/10.1016/j.ejca.2013.06.005
   PubMed Web of Science ®Google Scholar
• Zafirellis K, Zachaki A, Agrogiannis G, Gravani K. Inducible nitric oxide synthase expression and its prognostic significance in colorectal cancer. APMIS 2010; 118:115-24; PMID:20132175; http://dx.doi.org/10.1111/j.1600-0463.2009.02569.x
   PubMed Web of Science ®Google Scholar
• Forssell J, Oberg A, Henriksson ML, Stenling R, Jung A, Palmqvist R. High macrophage infiltration along the tumor front correlates with improved survival in colon cancer. Clin Cancer Res 2007; 13:1472-9; PMID:17332291; http://dx.doi.org/10.1158/1078-0432.CCR-06-2073
   PubMed Web of Science ®Google Scholar
• Algars A, Irjala H, Vaittinen S, Huhtinen H, Sundstrom J, Salmi M, Ristamaki R, Jalkanen S. Type and location of tumor-infiltrating macrophages and lymphatic vessels predict survival of colorectal cancer patients. Int J Cancer 2012; 131:864-73; PMID:21952788; http://dx.doi.org/10.1002/ijc.26457
   PubMed Web of Science ®Google Scholar
• Japink D, Leers MP, Sosef MN, Nap M. CEA in activated macrophages. New diagnostic possibilities for tumor markers in early colorectal cancer. Anticancer Res 2009; 29:3245-51; PMID:19661342
   PubMed Web of Science ®Google Scholar
• Edin S, Wikberg ML, Dahlin AM, Rutegard J, Oberg A, Oldenborg PA, Palmqvist R. The distribution of macrophages with a M1 or M2 phenotype in relation to prognosis and the molecular characteristics of colorectal cancer. PloS one 2012; 7:e47045; PMID:23077543; http://dx.doi.org/10.1371/journal.pone.0047045
   PubMed Web of Science ®Google Scholar
• Davis MJ, Tsang TM, Qiu Y, Dayrit JK, Freij JB, Huffnagle GB, Olszewski MA. Macrophage M1/M2 polarization dynamically adapts to changes in cytokine microenvironments in Cryptococcus neoformans infection. MBio 2013; 4:e00264-13; PMID:23781069; http://dx.doi.org/10.1128/mBio.00264-13
   PubMed Web of Science ®Google Scholar
• Nagorsen D, Voigt S, Berg E, Stein H, Thiel E, Loddenkemper C. Tumor-infiltrating macrophages and dendritic cells in human colorectal cancer: relation to local regulatory T cells, systemic T-cell response against tumor-associated antigens and survival. J Transl Med 2007; 5:62; PMID:18047662; http://dx.doi.org/10.1186/1479-5876-5-62
   PubMed Web of Science ®Google Scholar
• Edin S, Wikberg ML, Rutegard J, Oldenborg PA, Palmqvist R. Phenotypic skewing of macrophages in vitro by secreted factors from colorectal cancer cells. PloS one 2013; 8:e74982; PMID:24058644; http://dx.doi.org/10.1371/journal.pone.0074982
   PubMed Web of Science ®Google Scholar
• Banerjee A, Vasanthakumar A, Grigoriadis G. Modulating T regulatory cells in cancer: how close are we? Immunol Cell Biol 2013; 91:340-9; PMID:23567897; http://dx.doi.org/10.1038/icb.2013.12
   PubMed Web of Science ®Google Scholar
• Sobin LH, Gospodarowicz MK, Wittekind C, International Union against Cancer. TNM classification of malignant tumours. Chichester, West Sussex, UK; Hoboken, NJ: Wiley-Blackwell, 2010.
   Google Scholar
• Karamitopoulou E, Zlobec I, Kolzer V, Kondi-Pafiti A, Patsouris ES, Gennatas K, Lugli A. Proposal for a 10-high-power-fields scoring method for the assessment of tumor budding in colorectal cancer. Mod Pathol 2013; 26:295-301; PMID:23018875; http://dx.doi.org/10.1038/modpathol.2012.155
   PubMed Web of Science ®Google Scholar
• Horcic M, Koelzer VH, Karamitopoulou E, Terracciano L, Puppa G, Zlobec I, Lugli A. Tumor budding score based on 10 high-power fields is a promising basis for a standardized prognostic scoring system in stage II colorectal cancer. HumPathol 2013; 44:697-705; PMID:23159156; http://dx.doi.org/10.1016/j.humpath.2012.07.026
   Google Scholar
• Popat S, Houlston RS. Re: Reporting recommendations for tumor marker prognostic studies (REMARK). J Natl Cancer Inst 2005; 97:1855; author reply -6; PMID:16368950; http://dx.doi.org/10.1093/jnci/dji445
   PubMed Web of Science ®Google Scholar
• Zlobec I, Suter G, Perren A, Lugli A. A next-generation tissue microarray (ngTMA) protocol for biomarker studies. J Vis Exp 2014; 91:51893; 51893
   PubMed Web of Science ®Google Scholar
• Zlobec I, Koelzer VH, Dawson H, Perren A, Lugli A. Next-generation tissue microarray (ngTMA) increases the quality of biomarker studies: an example using CD3, CD8, and CD45RO in the tumor microenvironment of six different solid tumor types. J Transl Med 2013; 11:104; PMID:23627766; http://dx.doi.org/10.1186/1479-5876-11-104
   PubMed Web of Science ®Google Scholar
• Dawson H, Galvan JA, Helbling M, Muller DE, Karamitopoulou E, Koelzer VH, Economou M, Hammer C, Lugli A, Zlobec I. Possible role of Cdx2 in the serrated pathway of colorectal cancer characterized by BRAF mutation, high-level CpG Island methylator phenotype and mismatch repair-deficiency. Int J Cancer 2014; 134:2342-51; PMID:24166180; http://dx.doi.org/10.1002/ijc.28564
   PubMed Web of Science ®Google Scholar