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PMID: 21909876 Published · ppublish English Journal Article

Tumor-associated Macrophages (TAM) and Inflammation in Colorectal Cancer.

Cancer microenvironment : official journal of the International Cancer Microenvironment Society ·Vol. 4 ·No. 2 ·2011-08-00 ·Pages 141-54

Erreni M, Mantovani A, Allavena P

Abstract

Experimental and epidemiological studies indicate a strong link between chronic inflammation and tumor progression. Human colorectal cancer (CRC), a major cause of cancer-related death in Western countries, represents a paradigm for this link. Key features of cancer-related inflammation in CRC are the activation of transcription factors (e.g. NF-κB, STAT3), the expression of inflammatory cytokines and chemokines (e.g. TNFα, IL-6, CCL2, CXCL8) as well as a prominent leukocyte infiltrate. While considerable evidence indicates that the presence of lymphocytes of adaptive immunity may positively influence patient survival and clinical outcome in CRC, the role of tumor-associated macrophages (TAM) and of other lymphoid populations (e.g. Th17, Treg) is still unclear. In this review we will summarize the different and controversial effects that TAM play in CRC-related inflammation and progression of disease. The characterization of the most relevant inflammatory pathways in CRC is instrumental for the identification of new target molecules that could lead to improved diagnosis and treatment.

Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Erreni Marco
Department of Immunology and Inflammation, IRCCS Istituto Clinico Humanitas, Via Manzoni, 56, Rozzano, Milan, Italy.
Mantovani Alberto
Allavena Paola
References (168)
168 references, click to expand
  1. MMP-9 is differentially expressed in primary human colorectal adenocarcinomas and their metastases.
    Mol Cancer Res. 2006 May;4(5):293-302 PMID: 16687484
  2. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells.
    Nature. 2006 May 11;441(7090):235-8 PMID: 16648838
  3. IKKbeta links inflammation and tumorigenesis in a mouse model of colitis-associated cancer.
    Cell. 2004 Aug 6;118(3):285-96 PMID: 15294155
  4. Chemokine expression is associated with the accumulation of tumour associated macrophages (TAMs) and progression in human colorectal cancer.
    Clin Exp Metastasis. 2007;24(2):121-30 PMID: 17390111
  5. Local and distant recurrences in rectal cancer patients are predicted by the nonspecific immune response; specific immune response has only a systemic effect--a histopathological and immunohistochemical study.
    BMC Cancer. 2001;1:7 PMID: 11481031
  6. Regulation of the macrophage content of neoplasms by chemoattractants.
    Science. 1983 Apr 8;220(4593):210-2 PMID: 6828888
  7. Hereditary colorectal cancer.
    N Engl J Med. 2003 Mar 6;348(10):919-32 PMID: 12621137
  8. Chemokine receptor CXCR3 promotes colon cancer metastasis to lymph nodes.
    Oncogene. 2007 Jul 12;26(32):4679-88 PMID: 17297455
  9. Antitumor and anti-inflammatory effects of trabectedin on human myxoid liposarcoma cells.
    Cancer Res. 2010 Mar 15;70(6):2235-44 PMID: 20215499
  10. Intestinal inflammation in mice deficient in Tir8, an inhibitory member of the IL-1 receptor family.
    Proc Natl Acad Sci U S A. 2004 Mar 9;101(10):3522-6 PMID: 14993616
  11. Ras-induced interleukin-8 expression plays a critical role in tumor growth and angiogenesis.
    Cancer Cell. 2004 Nov;6(5):447-58 PMID: 15542429
  12. Chemokine receptor CXCR4 expression in colorectal cancer patients increases the risk for recurrence and for poor survival.
    J Clin Oncol. 2005 Apr 20;23(12):2744-53 PMID: 15837989
  13. Innate lymphoid cells drive interleukin-23-dependent innate intestinal pathology.
    Nature. 2010 Apr 29;464(7293):1371-5 PMID: 20393462
  14. IL-23 promotes tumour incidence and growth.
    Nature. 2006 Jul 27;442(7101):461-5 PMID: 16688182
  15. Intraepithelial CD8+ T-cell-count becomes a prognostic factor after a longer follow-up period in human colorectal carcinoma: possible association with suppression of micrometastasis.
    Br J Cancer. 2004 Nov 1;91(9):1711-7 PMID: 15494715
  16. The regulation of IL-10 production by immune cells.
    Nat Rev Immunol. 2010 Mar;10(3):170-81 PMID: 20154735
  17. Snail, Zeb and bHLH factors in tumour progression: an alliance against the epithelial phenotype?
    Nat Rev Cancer. 2007 Jun;7(6):415-28 PMID: 17508028
  18. Colorectal cancer and genetic alterations in the Wnt pathway.
    Oncogene. 2006 Dec 4;25(57):7531-7 PMID: 17143297
  19. Tumour-associated macrophages are a distinct M2 polarised population promoting tumour progression: potential targets of anti-cancer therapy.
    Eur J Cancer. 2006 Apr;42(6):717-27 PMID: 16520032
  20. Vascular endothelial growth factor, CD68, and epidermal growth factor receptor expression and survival in patients with Stage II and Stage III colon carcinoma: a role for the host response in prognosis.
    Cancer. 2003 Feb 15;97(4):960-8 PMID: 12569594
  21. Toll-like receptors on tumor cells facilitate evasion of immune surveillance.
    Cancer Res. 2005 Jun 15;65(12):5009-14 PMID: 15958541
  22. The interface between innate and adaptive immunity.
    Nat Immunol. 2004 Oct;5(10):971-4 PMID: 15454919
  23. Tumor-infiltrating FOXP3+ T regulatory cells show strong prognostic significance in colorectal cancer.
    J Clin Oncol. 2009 Jan 10;27(2):186-92 PMID: 19064967
  24. Cytokine repertoire during maturation of monocytes to macrophages within spheroids of malignant and non-malignant urothelial cell lines.
    Int J Cancer. 1998 Nov 23;78(5):648-53 PMID: 9808537
  25. Type, density, and location of immune cells within human colorectal tumors predict clinical outcome.
    Science. 2006 Sep 29;313(5795):1960-4 PMID: 17008531
  26. CD4+CD25+ regulatory lymphocytes induce regression of intestinal tumors in ApcMin/+ mice.
    Cancer Res. 2005 May 15;65(10):3998-4004 PMID: 15899788
  27. Regulation of immune responses by L-arginine metabolism.
    Nat Rev Immunol. 2005 Aug;5(8):641-54 PMID: 16056256
  28. gp130-mediated Stat3 activation in enterocytes regulates cell survival and cell-cycle progression during colitis-associated tumorigenesis.
    Cancer Cell. 2009 Feb 3;15(2):91-102 PMID: 19185844
  29. The origin and function of tumor-associated macrophages.
    Immunol Today. 1992 Jul;13(7):265-70 PMID: 1388654
  30. A review of gene-drug interactions for nonsteroidal anti-inflammatory drug use in preventing colorectal neoplasia.
    Pharmacogenomics J. 2008 Aug;8(4):237-47 PMID: 18195728
  31. Expression of costimulatory molecules B7-1 and B7-2 by macrophages along invasive margin of colon cancer: a possible antitumor immunity?
    Lab Invest. 1997 Sep;77(3):231-41 PMID: 9314947
  32. CXCL8 modulates human intestinal epithelial cells through a CXCR1 dependent pathway.
    Cytokine. 2005 Jan 7;29(1):42-8 PMID: 15579377
  33. Linking colorectal cancer to Wnt signaling.
    Cell. 2000 Oct 13;103(2):311-20 PMID: 11057903
  34. Identification of CD8+CD25+Foxp3+ suppressive T cells in colorectal cancer tissue.
    Gut. 2009 Apr;58(4):520-9 PMID: 19022917
  35. Direct evidence that bevacizumab, an anti-VEGF antibody, up-regulates SDF1alpha, CXCR4, CXCL6, and neuropilin 1 in tumors from patients with rectal cancer.
    Cancer Res. 2009 Oct 15;69(20):7905-10 PMID: 19826039
  36. The genetics of hereditary colon cancer.
    Genes Dev. 2007 Oct 15;21(20):2525-38 PMID: 17938238
  37. TGF-beta and cancer.
    Cytokine Growth Factor Rev. 2006 Feb-Apr;17(1-2):29-40 PMID: 16289860
  38. Blockade of a chemokine, CCL2, reduces chronic colitis-associated carcinogenesis in mice.
    Cancer Res. 2009 Oct 1;69(19):7884-92 PMID: 19773434
  39. Prediction of lymph node metastasis in colorectal carcinoma by expressionof chemokine receptor CCR7.
    Int J Cancer. 2005 Sep 20;116(5):726-33 PMID: 15828050
  40. Sulfated glycosphingolipid as mediator of phagocytosis: SM4s enhances apoptotic cell clearance and modulates macrophage activity.
    J Immunol. 2007 Nov 15;179(10):6770-82 PMID: 17982067
  41. Endogenous IL-17 contributes to reduced tumor growth and metastasis.
    Blood. 2009 Jul 9;114(2):357-9 PMID: 19289853
  42. High expression of Foxp3, IL-23p19 and survivin mRNA in colorectal carcinoma.
    Int J Colorectal Dis. 2009 Feb;24(2):151-7 PMID: 18825388
  43. The role of chemokines in intestinal inflammation and cancer.
    Curr Opin Pharmacol. 2009 Dec;9(6):688-96 PMID: 19734090
  44. Colorectal cancer.
    Lancet. 2005 Jan 8-14;365(9454):153-65 PMID: 15639298
  45. Induction of a proinflammatory program in normal human thyrocytes by the RET/PTC1 oncogene.
    Proc Natl Acad Sci U S A. 2005 Oct 11;102(41):14825-30 PMID: 16203990
  46. Histologic inflammation is a risk factor for progression to colorectal neoplasia in ulcerative colitis: a cohort study.
    Gastroenterology. 2007 Oct;133(4):1099-105; quiz 1340-1 PMID: 17919486
  47. Effect of aspirin on long-term risk of colorectal cancer: consistent evidence from randomised and observational studies.
    Lancet. 2007 May 12;369(9573):1603-13 PMID: 17499602
  48. IL-23 drives a pathogenic T cell population that induces autoimmune inflammation.
    J Exp Med. 2005 Jan 17;201(2):233-40 PMID: 15657292
  49. Prognostic role of CD8+ tumor-infiltrating lymphocytes in stage III colorectal cancer with and without microsatellite instability.
    Hum Pathol. 2004 Jul;35(7):808-16 PMID: 15257543
  50. Myeloid-derived suppressor cells as regulators of the immune system.
    Nat Rev Immunol. 2009 Mar;9(3):162-74 PMID: 19197294
  51. Loss of Smad4 correlates with loss of the invasion suppressor E-cadherin in advanced colorectal carcinomas.
    J Pathol. 2004 Apr;202(4):412-20 PMID: 15095268
  52. Aspirin and the risk of colorectal cancer in relation to the expression of COX-2.
    N Engl J Med. 2007 May 24;356(21):2131-42 PMID: 17522398
  53. 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
  54. Suppression of tumor formation in vivo by expression of the JE gene in malignant cells.
    Mol Cell Biol. 1991 Jun;11(6):3125-31 PMID: 2038321
  55. The chemokine CCL5 as a potential prognostic factor predicting disease progression in stage II breast cancer patients.
    Clin Cancer Res. 2006 Aug 1;12(15):4474-80 PMID: 16899591
  56. Macrophage polarization comes of age.
    Immunity. 2005 Oct;23(4):344-6 PMID: 16226499
  57. Immune cells as mediators of solid tumor metastasis.
    Cancer Metastasis Rev. 2008 Mar;27(1):11-8 PMID: 18066650
  58. Mismatch repair and the hereditary non-polyposis colorectal cancer syndrome (HNPCC).
    Cancer Invest. 2002;20(1):102-9 PMID: 11852992
  59. Tumor-associated macrophages in neoplastic progression: a paradigm for the in vivo function of chemokines.
    Lab Invest. 1994 Jul;71(1):5-16 PMID: 7518882
  60. Regulation of the chemokine receptor CXCR4 by hypoxia.
    J Exp Med. 2003 Nov 3;198(9):1391-402 PMID: 14597738
  61. Genetic alterations in locally advanced stage II/III colon cancer: a search for prognostic markers.
    Clin Colorectal Cancer. 2004 Nov;4(4):252-9 PMID: 15555207
  62. Aspirin, COX-2, and the risk of colorectal cancer.
    N Engl J Med. 2007 Aug 23;357(8):824-5; author reply 824-5 PMID: 17715417
  63. Alternative activation of macrophages.
    Nat Rev Immunol. 2003 Jan;3(1):23-35 PMID: 12511873
  64. The genetics of colorectal cancer.
    Ann Intern Med. 2002 Oct 1;137(7):603-12 PMID: 12353948
  65. NF-kappaB: linking inflammation and immunity to cancer development and progression.
    Nat Rev Immunol. 2005 Oct;5(10):749-59 PMID: 16175180
  66. Macrophages: obligate partners for tumor cell migration, invasion, and metastasis.
    Cell. 2006 Jan 27;124(2):263-6 PMID: 16439202
  67. Direct visualization of macrophage-assisted tumor cell intravasation in mammary tumors.
    Cancer Res. 2007 Mar 15;67(6):2649-56 PMID: 17363585
  68. Induction of systemic immunity by expression of interleukin-23 in murine colon carcinoma cells.
    Int J Cancer. 2003 Jul 20;105(6):820-4 PMID: 12767068
  69. Inflammation and cancer: IL-6 and STAT3 complete the link.
    Cancer Cell. 2009 Feb 3;15(2):79-80 PMID: 19185839
  70. The prognostic significance of intratumoral natural killer cells in patients with colorectal carcinoma.
    Cancer. 1997 Jun 15;79(12):2320-8 PMID: 9191519
  71. Regulation of leukocyte binding to endothelial tissues by tumor-derived GM-CSF.
    Int J Cancer. 1992 Feb 20;50(4):585-8 PMID: 1537624
  72. High macrophage infiltration along the tumor front correlates with improved survival in colon cancer.
    Clin Cancer Res. 2007 Mar 1;13(5):1472-9 PMID: 17332291
  73. Cancer risk in patients with inflammatory bowel disease: a population-based study.
    Cancer. 2001 Feb 15;91(4):854-62 PMID: 11241255
  74. CXCL10 promotes invasion-related properties in human colorectal carcinoma cells.
    Cancer Res. 2007 Apr 1;67(7):3396-405 PMID: 17409450
  75. Tumor-associated macrophages and the related myeloid-derived suppressor cells as a paradigm of the diversity of macrophage activation.
    Hum Immunol. 2009 May;70(5):325-30 PMID: 19236898
  76. Increased susceptibility to colitis-associated cancer of mice lacking TIR8, an inhibitory member of the interleukin-1 receptor family.
    Cancer Res. 2007 Jul 1;67(13):6017-21 PMID: 17616656
  77. Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma.
    Cancer Res. 1996 Oct 15;56(20):4625-9 PMID: 8840975
  78. The relationship between tumour T-lymphocyte infiltration, the systemic inflammatory response and survival in patients undergoing curative resection for colorectal cancer.
    Br J Cancer. 2005 Feb 28;92(4):651-4 PMID: 15700032
  79. Human anti-inflammatory macrophages induce Foxp3+ GITR+ CD25+ regulatory T cells, which suppress via membrane-bound TGFbeta-1.
    J Immunol. 2008 Aug 1;181(3):2220-6 PMID: 18641362
  80. Regulatory T cells in cancer.
    Adv Cancer Res. 2010;107:57-117 PMID: 20399961
  81. Chronic pancreatitis is essential for induction of pancreatic ductal adenocarcinoma by K-Ras oncogenes in adult mice.
    Cancer Cell. 2007 Mar;11(3):291-302 PMID: 17349585
  82. The inflammatory micro-environment in tumor progression: the role of tumor-associated macrophages.
    Crit Rev Oncol Hematol. 2008 Apr;66(1):1-9 PMID: 17913510
  83. Interleukin-22-producing natural killer cells and lymphoid tissue inducer-like cells in mucosal immunity.
    Immunity. 2009 Jul 17;31(1):15-23 PMID: 19604490
  84. The lymphatic system controls intestinal inflammation and inflammation-associated Colon Cancer through the chemokine decoy receptor D6.
    Gut. 2010 Feb;59(2):197-206 PMID: 19846409
  85. The differentiation of human T(H)-17 cells requires transforming growth factor-beta and induction of the nuclear receptor RORgammat.
    Nat Immunol. 2008 Jun;9(6):641-9 PMID: 18454151
  86. Blocking TNF-alpha in mice reduces colorectal carcinogenesis associated with chronic colitis.
    J Clin Invest. 2008 Feb;118(2):560-70 PMID: 18219394
  87. Cancer and the chemokine network.
    Nat Rev Cancer. 2004 Jul;4(7):540-50 PMID: 15229479
  88. Chemokine receptor CXCR4 downregulated by von Hippel-Lindau tumour suppressor pVHL.
    Nature. 2003 Sep 18;425(6955):307-11 PMID: 13679920
  89. IL-6 and Stat3 are required for survival of intestinal epithelial cells and development of colitis-associated cancer.
    Cancer Cell. 2009 Feb 3;15(2):103-13 PMID: 19185845
  90. VEGFR1-positive haematopoietic bone marrow progenitors initiate the pre-metastatic niche.
    Nature. 2005 Dec 8;438(7069):820-7 PMID: 16341007
  91. Differential regulation of chemokines by IL-17 in colonic epithelial cells.
    J Immunol. 2008 Nov 1;181(9):6536-45 PMID: 18941244
  92. Chemotactic factors, passive invasion and metastasis of cancer cells.
    Immunol Today. 1992 Nov;13(11):463-4 PMID: 1298279
  93. Interleukin-6: from basic science to medicine--40 years in immunology.
    Annu Rev Immunol. 2005;23:1-21 PMID: 15771564
  94. Extracellular and intracellular decoys in the tuning of inflammatory cytokines and Toll-like receptors: the new entry TIR8/SIGIRR.
    J Leukoc Biol. 2004 May;75(5):738-42 PMID: 14673019
  95. Other functions, other genes: alternative activation of antigen-presenting cells.
    Immunity. 1999 Feb;10(2):137-42 PMID: 10072066
  96. Regulatory lymphocytes and intestinal inflammation.
    Annu Rev Immunol. 2009;27:313-38 PMID: 19302043
  97. SIGIRR, a negative regulator of Toll-like receptor-interleukin 1 receptor signaling.
    Nat Immunol. 2003 Sep;4(9):920-7 PMID: 12925853
  98. Tumour-associated leucocytes: friends or foes in breast carcinoma.
    J Pathol. 1994 Mar;172(3):229-35 PMID: 8195926
  99. Unique pattern of expression and inhibition of IL-1 signaling by the IL-1 receptor family member TIR8/SIGIRR.
    Eur Cytokine Netw. 2003 Oct-Dec;14(4):211-8 PMID: 14715412
  100. Macrophage polarization: tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes.
    Trends Immunol. 2002 Nov;23(11):549-55 PMID: 12401408
  101. Tuning inflammation and immunity by chemokine sequestration: decoys and more.
    Nat Rev Immunol. 2006 Dec;6(12):907-18 PMID: 17124512
  102. Mast cells are an essential hematopoietic component for polyp development.
    Proc Natl Acad Sci U S A. 2007 Dec 11;104(50):19977-82 PMID: 18077429
  103. Diagnosis and management of dysplasia in patients with inflammatory bowel diseases.
    Gastroenterology. 2004 May;126(6):1634-48 PMID: 15168373
  104. TGFbeta in Cancer.
    Cell. 2008 Jul 25;134(2):215-30 PMID: 18662538
  105. The NF-κB/AKT-dependent Induction of Wnt Signaling in Colon Cancer Cells by Macrophages and IL-1β.
    Cancer Microenviron. 2009 Sep 25;2(1):69-80 PMID: 19779850
  106. The Myc-dependent angiogenic switch in tumors is mediated by interleukin 1beta.
    Genes Dev. 2006 Sep 15;20(18):2527-38 PMID: 16980582
  107. Cyclooxygenase polymorphisms in gastric and colorectal carcinogenesis: are conclusive results available?
    Eur J Gastroenterol Hepatol. 2009 Jan;21(1):76-91 PMID: 19060633
  108. Effector memory T cells, early metastasis, and survival in colorectal cancer.
    N Engl J Med. 2005 Dec 22;353(25):2654-66 PMID: 16371631
  109. The BRAF-MAPK signaling pathway is essential for cancer-immune evasion in human melanoma cells.
    J Exp Med. 2006 Jul 10;203(7):1651-6 PMID: 16801397
  110. Cancer-related inflammation.
    Nature. 2008 Jul 24;454(7203):436-44 PMID: 18650914
  111. Colorectal cancers with microsatellite instability display mRNA expression signatures characteristic of increased immunogenicity.
    Mol Cancer. 2004 Aug 06;3:21 PMID: 15298707
  112. Inflammation and cancer: back to Virchow?
    Lancet. 2001 Feb 17;357(9255):539-45 PMID: 11229684
  113. TGF-beta indirectly favors the development of human Th17 cells by inhibiting Th1 cells.
    Eur J Immunol. 2009 Jan;39(1):207-15 PMID: 19130583
  114. CD8+ T cells infiltrated within cancer cell nests as a prognostic factor in human colorectal cancer.
    Cancer Res. 1998 Aug 15;58(16):3491-4 PMID: 9721846
  115. CD3+ cells at the invasive margin of deeply invading (pT3-T4) colorectal cancer and risk of post-surgical metastasis: a longitudinal study.
    Lancet Oncol. 2009 Sep;10(9):877-84 PMID: 19656725
  116. Identification and characterization of SIGIRR, a molecule representing a novel subtype of the IL-1R superfamily.
    Cytokine. 1999 Jun;11(6):389-99 PMID: 10346978
  117. The tumor microenvironment: the making of a paradigm.
    Cancer Microenviron. 2009 Sep;2 Suppl 1:9-17 PMID: 19701697
  118. The degree of macrophage infiltration into the cancer cell nest is a significant predictor of survival in gastric cancer patients.
    Anticancer Res. 2003 Nov-Dec;23(6D):5015-22 PMID: 14981961
  119. Expression of chemokines and chemokine receptors in human colon cancer.
    Methods Enzymol. 2009;460:105-21 PMID: 19446722
  120. Activated macrophages induce metastatic behavior of colon cancer cells.
    Immunobiology. 2010 Mar;215(3):242-9 PMID: 19457576
  121. Reduced likelihood of metastases in patients with microsatellite-unstable colorectal cancer.
    Clin Cancer Res. 2007 Jul 1;13(13):3831-9 PMID: 17606714
  122. Interplay between IFN-gamma and IL-6 signaling governs neutrophil trafficking and apoptosis during acute inflammation.
    J Clin Invest. 2003 Aug;112(4):598-607 PMID: 12925700
  123. Smoldering and polarized inflammation in the initiation and promotion of malignant disease.
    Cancer Cell. 2005 Mar;7(3):211-7 PMID: 15766659
  124. Inflammation and colon cancer.
    Gastroenterology. 2010 Jun;138(6):2101-2114.e5 PMID: 20420949
  125. Natural killer cells infiltrating colorectal cancer and MHC class I expression.
    Mol Immunol. 2005 Feb;42(4):541-6 PMID: 15607811
  126. Regulation of spontaneous intestinal tumorigenesis through the adaptor protein MyD88.
    Science. 2007 Jul 6;317(5834):124-7 PMID: 17615359
  127. Preparing the "soil": the premetastatic niche.
    Cancer Res. 2006 Dec 1;66(23):11089-93 PMID: 17145848
  128. The altered tumoricidal capacity of macrophages isolated from tumor-bearing mice is related to reduce expression of the inducible nitric oxide synthase gene.
    J Exp Med. 1996 Apr 1;183(4):1323-9 PMID: 8666890
  129. Interleukin-6 stimulates clonogenic growth of primary and metastatic human colon carcinoma cells.
    Cancer Lett. 2000 Apr 3;151(1):31-8 PMID: 10766420
  130. TGFbeta1, a "Jack of all trades": the link with pro-inflammatory IL-17-producing T cells.
    Trends Immunol. 2006 Aug;27(8):358-61 PMID: 16793343
  131. Is colony-stimulating factor-1 a key mediator of breast cancer invasion and metastasis?
    Mol Carcinog. 1993;7(4):207-11 PMID: 8352880
  132. Effect of COX2 -765G>C and c.3618A>G polymorphisms on the risk and survival of sporadic colorectal cancer.
    Cancer Causes Control. 2009 Oct;20(8):1421-9 PMID: 19468846
  133. The Role of Inflammation in the Pathogenesis of Colorectal Cancer.
    Curr Colorectal Cancer Rep. 2009 Apr 1;5(2):69-74 PMID: 19756239
  134. Recruitment of STAT3 for production of IL-10 by colon carcinoma cells induced by macrophage-derived IL-6.
    J Immunol. 2004 Apr 1;172(7):4630-6 PMID: 15034082
  135. Vascular endothelial growth factor secretion by tumor-infiltrating macrophages essentially supports tumor angiogenesis, and IgG immune complexes potentiate the process.
    Cancer Res. 2002 Dec 1;62(23):7042-9 PMID: 12460925
  136. Transforming growth factor-beta employs HMGA2 to elicit epithelial-mesenchymal transition.
    J Cell Biol. 2006 Jul 17;174(2):175-83 PMID: 16831886
  137. Close association between Fas ligand (FasL; CD95L)-positive tumor-associated macrophages and apoptotic cancer cells along invasive margin of colorectal carcinoma: a proposal on tumor-host interactions.
    Jpn J Cancer Res. 2002 Mar;93(3):320-8 PMID: 11927015
  138. Microsatellite instability in colorectal cancer.
    Br J Surg. 2006 Apr;93(4):395-406 PMID: 16555243
  139. Inflammatory cell infiltration of tumors: Jekyll or Hyde.
    Cancer Metastasis Rev. 2007 Dec;26(3-4):373-400 PMID: 17717638
  140. Transforming growth factor beta is dispensable for the molecular orchestration of Th17 cell differentiation.
    J Exp Med. 2009 Oct 26;206(11):2407-16 PMID: 19808254
  141. Interleukins 1beta and 6 but not transforming growth factor-beta are essential for the differentiation of interleukin 17-producing human T helper cells.
    Nat Immunol. 2007 Sep;8(9):942-9 PMID: 17676045
  142. Role of tumor-associated macrophages in tumor progression and invasion.
    Cancer Metastasis Rev. 2006 Sep;25(3):315-22 PMID: 16967326
  143. The density of macrophages in the invasive front is inversely correlated to liver metastasis in colon cancer.
    J Transl Med. 2010 Feb 08;8:13 PMID: 20141634
  144. Live imaging of cysteine-cathepsin activity reveals dynamics of focal inflammation, angiogenesis, and polyp growth.
    PLoS One. 2008 Aug 13;3(8):e2916 PMID: 18698347
  145. Role of Toll-like receptors in gastrointestinal malignancies.
    Oncogene. 2008 Jan 7;27(2):234-43 PMID: 18176605
  146. Cross-talk between myeloid-derived suppressor cells and macrophages subverts tumor immunity toward a type 2 response.
    J Immunol. 2007 Jul 15;179(2):977-83 PMID: 17617589
  147. Prognostic influence of tumor-associated eosinophilic infiltrate in colorectal carcinoma.
    Cancer. 2000 Apr 1;88(7):1544-8 PMID: 10738211
  148. High prevalence of activated intraepithelial cytotoxic T lymphocytes and increased neoplastic cell apoptosis in colorectal carcinomas with microsatellite instability.
    Am J Pathol. 1999 Jun;154(6):1805-13 PMID: 10362805
  149. The three Es of cancer immunoediting.
    Annu Rev Immunol. 2004;22:329-60 PMID: 15032581
  150. Gender difference for promoter methylation pattern of hMLH1 and p16 in sporadic MSI colorectal cancer.
    Gastroenterology. 2003 Apr;124(4):1165-6 PMID: 12671921
  151. Tumour-educated macrophages promote tumour progression and metastasis.
    Nat Rev Cancer. 2004 Jan;4(1):71-8 PMID: 14708027
  152. Serum interleukin-6 levels in colorectal cancer patients--a summary of published results.
    Int J Colorectal Dis. 2010 Feb;25(2):135-40 PMID: 19898853
  153. Monocyte and macrophage heterogeneity.
    Nat Rev Immunol. 2005 Dec;5(12):953-64 PMID: 16322748
  154. NF-kappaB functions as a tumour promoter in inflammation-associated cancer.
    Nature. 2004 Sep 23;431(7007):461-6 PMID: 15329734
  155. DNA damage induced by chronic inflammation contributes to colon carcinogenesis in mice.
    J Clin Invest. 2008 Jul;118(7):2516-25 PMID: 18521188
  156. Effect of chemokine receptors CXCR4 and CCR7 on the metastatic behavior of human colorectal cancer.
    Clin Cancer Res. 2005 Mar 1;11(5):1743-50 PMID: 15755995
  157. Influence of interleukin-6 on the invasiveness of human colorectal carcinoma.
    Anticancer Res. 2006 Nov-Dec;26(6B):4607-14 PMID: 17201185
  158. In situ analysis of FOXP3+ regulatory T cells in human colorectal cancer.
    J Transl Med. 2006 Dec 13;4:52 PMID: 17166272
  159. Differentiation-dependent expression and mitogenic action of interleukin-6 in human colon carcinoma cells: relevance for tumour progression.
    Eur J Cancer. 2005 Oct;41(15):2347-54 PMID: 16176872
  160. The terminology issue for myeloid-derived suppressor cells.
    Cancer Res. 2007 Jan 1;67(1):425; author reply 426 PMID: 17210725
  161. Tumor-associated macrophages and survival in classic Hodgkin's lymphoma.
    N Engl J Med. 2010 Mar 11;362(10):875-85 PMID: 20220182
  162. Gender disparity in liver cancer due to sex differences in MyD88-dependent IL-6 production.
    Science. 2007 Jul 6;317(5834):121-4 PMID: 17615358
  163. Celecoxib for the prevention of colorectal adenomatous polyps.
    N Engl J Med. 2006 Aug 31;355(9):885-95 PMID: 16943401
  164. Tumour necrosis factor and cancer.
    Nat Rev Cancer. 2009 May;9(5):361-71 PMID: 19343034
  165. Plasticity of macrophage function during tumor progression: regulation by distinct molecular mechanisms.
    J Immunol. 2008 Feb 15;180(4):2011-7 PMID: 18250403
  166. Prognostic significance of CD8+ T cell and macrophage peritumoral infiltration in colorectal cancer.
    Oncol Rep. 2003 Mar-Apr;10(2):309-13 PMID: 12579264
  167. Blockade of interleukin 6 trans signaling suppresses T-cell resistance against apoptosis in chronic intestinal inflammation: evidence in crohn disease and experimental colitis in vivo.
    Nat Med. 2000 May;6(5):583-8 PMID: 10802717
  168. Reduced beta-catenin and peroxisome proliferator-activated receptor-gamma expression levels are associated with colorectal cancer metastatic progression: correlation with tumor-associated macrophages, cyclooxygenase 2, and patient outcome.
    Hum Pathol. 2009 May;40(5):714-25 PMID: 19121846
Article Info
Journal
Cancer microenvironment : official journal of the International Cancer Microenvironment Society
Abbr.
Cancer Microenviron
ISSN
1875-2284
DOI
10.1007/s12307-010-0052-5
Published
2011-08-00
Epub
2010-00-17
Pages
141-54
Language
English
Region
Netherlands
NLM ID
101322634
PMCID
PMC3170420
External Links
PubMed source DOI: 10.1007/s12307-010-0052-5 PMC Full Text
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