Immune cells: plastic players along colorectal cancer progression

Inflammatory cells are involved in tumour initiation and progression. In parallel, the adaptive immune response plays a key role in fighting tumour growth and dissemination. The double‐edged role of the immune system in solid tumours is well represented in colorectal cancer (CRC). The development and progression of CRC are affected by the interactions between the tumour and the host's response, occurring in a milieu named tumour microenvironment. The role of immune cells in human CRC is being unravelled and there is a strong interest in understanding their dynamics as to tumour promotion, immunosurveillance and immunoevasion. A better definition of immune infiltration would be important not only with respect to the ‘natural history’ of CRC, but in a clinically relevant perspective in the 21st century, with respect to its post‐surgical management, including chemotherapy responsiveness. While it is becoming established that the amount of tumour‐infiltrating lymphocytes influences the post‐surgical progression of early‐stage CRC, the relevance of this immune parameter as to chemotherapy responsiveness remains to be clarified. Despite recent experimental work supporting the notion that infiltrating immune cells may influence chemotherapy‐mediated tumour cell death, tumour‐infiltrating cells are not employed to identify patients who are more likely to benefit from adjuvant treatment. This review focuses on studies addressing the role of innate and adaptive immune cells along the occurrence and the progression of potentially curable CRC.

[1]  Bhanu P. Jena,et al.  Journal of Cellular and Molecular Medicine , 2014, Journal of Cellular and Molecular Medicine.

[2]  Fabio Grizzi,et al.  Prognostic value of innate and adaptive immunity in colorectal cancer. , 2013, World journal of gastroenterology.

[3]  Reiko Nishihara,et al.  Aspirin use, tumor PIK3CA mutation, and colorectal-cancer survival. , 2012, The New England journal of medicine.

[4]  F. Marincola,et al.  Cancer classification using the Immunoscore: a worldwide task force , 2012, Journal of Translational Medicine.

[5]  R. Ali,et al.  Aspirin as adjuvant therapy for colorectal cancer—reinterpreting paradigms , 2012, Nature Reviews Clinical Oncology.

[6]  Douglas G Altman,et al.  Reporting recommendations for tumor marker prognostic studies (REMARK): explanation and elaboration , 2012, BMC Medicine.

[7]  H. Ueno,et al.  Optimal colorectal cancer staging criteria in TNM classification. , 2012, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[8]  M. Thun,et al.  The role of aspirin in cancer prevention , 2012, Nature Reviews Clinical Oncology.

[9]  P. Rothwell,et al.  Effects of regular aspirin on long-term cancer incidence and metastasis: a systematic comparison of evidence from observational studies versus randomised trials. , 2012, The Lancet. Oncology.

[10]  S. Waldman,et al.  Molecular staging individualizing cancer management , 2012, Journal of surgical oncology.

[11]  C. Sautès-Fridman,et al.  The immune contexture in human tumours: impact on clinical outcome , 2012, Nature Reviews Cancer.

[12]  Axel Benner,et al.  Localization and density of immune cells in the invasive margin of human colorectal cancer liver metastases are prognostic for response to chemotherapy. , 2011, Cancer research.

[13]  G. Kroemer,et al.  Prognostic and predictive impact of intra- and peritumoral immune infiltrates. , 2011, Cancer research.

[14]  Maureen A. Smith,et al.  Adjuvant chemotherapy for stage II colon cancer with poor prognostic features. , 2011, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[15]  G. Dranoff,et al.  Cancer immunology—analysis of host and tumor factors for personalized medicine , 2011, Nature Reviews Clinical Oncology.

[16]  R. Labianca,et al.  DNA mismatch repair status and colon cancer recurrence and survival in clinical trials of 5-fluorouracil-based adjuvant therapy. , 2011, Journal of the National Cancer Institute.

[17]  R. Palmqvist,et al.  Colorectal cancer prognosis depends on T-cell infiltration and molecular characteristics of the tumor , 2011, Modern Pathology.

[18]  R. Schreiber,et al.  Natural innate and adaptive immunity to cancer. , 2011, Annual review of immunology.

[19]  D. Hanahan,et al.  Hallmarks of Cancer: The Next Generation , 2011, Cell.

[20]  Laurence Zitvogel,et al.  Immune parameters affecting the efficacy of chemotherapeutic regimens , 2011, Nature Reviews Clinical Oncology.

[21]  E. Giovannucci,et al.  Inflammatory markers are associated with risk of colorectal cancer and chemopreventive response to anti-inflammatory drugs. , 2011, Gastroenterology.

[22]  Zlatko Trajanoski,et al.  Histopathologic-based prognostic factors of colorectal cancers are associated with the state of the local immune reaction. , 2011, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[23]  Charles Chan,et al.  Clinicopathological staging of colorectal cancer: Evolution and consensus—an Australian perspective , 2011, Journal of gastroenterology and hepatology.

[24]  C. Mathers,et al.  Estimates of worldwide burden of cancer in 2008: GLOBOCAN 2008 , 2010, International journal of cancer.

[25]  Shuji Ogino,et al.  Tumour‐infiltrating T‐cell subsets, molecular changes in colorectal cancer, and prognosis: cohort study and literature review , 2010, The Journal of pathology.

[26]  C. Garlanda,et al.  The tumor microenvironment of colorectal cancer: stromal TLR-4 expression as a potential prognostic marker , 2010, Journal of Translational Medicine.

[27]  R. Labianca,et al.  Defective mismatch repair as a predictive marker for lack of efficacy of fluorouracil-based adjuvant therapy in colon cancer. , 2010, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[28]  Michael Karin,et al.  Inflammation and colon cancer. , 2010, Gastroenterology.

[29]  A. Lièvre,et al.  Oncogenic mutations as predictive factors in colorectal cancer , 2010, Oncogene.

[30]  M. Karin,et al.  Immunity, Inflammation, and Cancer , 2010, Cell.

[31]  J. Pignon,et al.  Immunogenic death of colon cancer cells treated with oxaliplatin , 2010, Oncogene.

[32]  Jun Hee Lee,et al.  Dietary and Genetic Obesity Promote Liver Inflammation and Tumorigenesis by Enhancing IL-6 and TNF Expression , 2010, Cell.

[33]  M. Karin,et al.  Tobacco smoke promotes lung tumorigenesis by triggering IKKbeta- and JNK1-dependent inflammation. , 2010, Cancer cell.

[34]  Zlatko Trajanoski,et al.  In situ cytotoxic and memory T cells predict outcome in patients with early-stage colorectal cancer. , 2009, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[35]  Hua Yu,et al.  STATs in cancer inflammation and immunity: a leading role for STAT3 , 2009, Nature Reviews Cancer.

[36]  Mari Mino-Kenudson,et al.  Lymphocytic Reaction to Colorectal Cancer Is Associated with Longer Survival, Independent of Lymph Node Count, Microsatellite Instability, and CpG Island Methylator Phenotype , 2009, Clinical Cancer Research.

[37]  V. Torri,et al.  CD3+ cells at the invasive margin of deeply invading (pT3-T4) colorectal cancer and risk of post-surgical metastasis: a longitudinal study. , 2009, The Lancet. Oncology.

[38]  P. Kosmidis,et al.  Colorectal cancer and inflammatory bowel disease: epidemiology, risk factors, mechanisms of carcinogenesis and prevention strategies. , 2009, Anticancer research.

[39]  M. Omata,et al.  Constitutive NF-κB Activation in Colorectal Carcinoma Plays a Key Role in Angiogenesis, Promoting Tumor Growth , 2009, Clinical Cancer Research.

[40]  B. Aggarwal,et al.  Targeting Inflammatory Pathways for Prevention and Therapy of Cancer: Short-Term Friend, Long-Term Foe , 2009, Clinical Cancer Research.

[41]  N. Zeps,et al.  Tumor-infiltrating FOXP3+ T regulatory cells show strong prognostic significance in colorectal cancer. , 2009, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[42]  P. Allavena,et al.  Cancer-related inflammation , 2008, Nature.

[43]  M. Neurath,et al.  Immune cells in colorectal cancer: prognostic relevance and therapeutic strategies , 2008, Expert review of anticancer therapy.

[44]  F. Marincola,et al.  Tumour immunity: effector response to tumour and role of the microenvironment , 2008, The Lancet.

[45]  B. Iacopetta,et al.  Tumor-Infiltrating Lymphocytes and Perforation in Colon Cancer Predict Positive Response to 5-Fluorouracil Chemotherapy , 2008, Clinical Cancer Research.

[46]  Lloyd J. Old,et al.  Adaptive immunity maintains occult cancer in an equilibrium state , 2007, Nature.

[47]  L. Zitvogel,et al.  The interaction between HMGB1 and TLR4 dictates the outcome of anticancer chemotherapy and radiotherapy , 2007, Immunological reviews.

[48]  T. Godfrey,et al.  Is occult lymph node disease in colorectal cancer patients clinically significant? A review of the relevant literature. , 2007, The Journal of molecular diagnostics : JMD.

[49]  Georgia Salanti,et al.  Survival and disease-progression benefits with treatment regimens for advanced colorectal cancer: a meta-analysis. , 2007, The Lancet. Oncology.

[50]  Laurence Zitvogel,et al.  Toll-like receptor 4–dependent contribution of the immune system to anticancer chemotherapy and radiotherapy , 2007, Nature Medicine.

[51]  V. Torri,et al.  Reduced Likelihood of Metastases in Patients with Microsatellite-Unstable Colorectal Cancer , 2007, Clinical Cancer Research.

[52]  M. Neurath,et al.  The T-box transcription factor eomesodermin controls CD8 T cell activity and lymph node metastasis in human colorectal cancer , 2007, Gut.

[53]  P. Rothwell,et al.  Effect of aspirin on long-term risk of colorectal cancer: consistent evidence from randomised and observational studies , 2007, The Lancet.

[54]  M. Koch,et al.  Tumor Infiltrating T Lymphocytes in Colorectal Cancer: Tumor-Selective Activation and Cytotoxic Activity In Situ , 2006, Annals of surgery.

[55]  Z. Trajanoski,et al.  Type, Density, and Location of Immune Cells Within Human Colorectal Tumors Predict Clinical Outcome , 2006, Science.

[56]  D. Parkin,et al.  The global health burden of infection‐associated cancers in the year 2002 , 2006, International journal of cancer.

[57]  K R Abrams,et al.  Meta‐analysis: colorectal and small bowel cancer risk in patients with Crohn's disease , 2006, Alimentary pharmacology & therapeutics.

[58]  J. Beebe-Dimmer,et al.  Chronic Inflammation: A Common and Important Factor in the Pathogenesis of Neoplasia , 2006, CA: a cancer journal for clinicians.

[59]  Z. Trajanoski,et al.  Effector memory T cells, early metastasis, and survival in colorectal cancer. , 2005, The New England journal of medicine.

[60]  C. Boland,et al.  Serrated Adenomas Have a Pattern of Genetic Alterations That Distinguishes Them from Other Colorectal Polyps , 2005, Cancer Epidemiology Biomarkers & Prevention.

[61]  M. Caraglia,et al.  Dendritic Cell-Mediated Cross-Presentation of Antigens Derived from Colon Carcinoma Cells Exposed to a Highly Cytotoxic Multidrug Regimen with Gemcitabine, Oxaliplatin, 5-Fluorouracil, and Leucovorin, Elicits a Powerful Human Antigen-Specific CTL Response with Antitumor Activity in Vitro1 , 2005, The Journal of Immunology.

[62]  B. Robinson,et al.  Immunotherapy and chemotherapy — a practical partnership , 2005, Nature Reviews Cancer.

[63]  C. Ko,et al.  Colon cancer survival rates with the new American Joint Committee on Cancer sixth edition staging. , 2005, Journal of the National Cancer Institute.

[64]  Hans Clevers,et al.  At the Crossroads of Inflammation and Cancer , 2004, Cell.

[65]  C. Ostwald,et al.  Prognostic role of CD8+ tumor-infiltrating lymphocytes in stage III colorectal cancer with and without microsatellite instability. , 2004, Human pathology.

[66]  G. Beck,et al.  A randomized trial of aspirin to prevent colorectal adenomas. , 2003, The New England journal of medicine.

[67]  R. MacKie,et al.  Fatal melanoma transferred in a donated kidney 16 years after melanoma surgery. , 2003, The New England journal of medicine.

[68]  R. Schreiber,et al.  Cancer immunoediting: from immunosurveillance to tumor escape , 2002, Nature Immunology.

[69]  C. Begg,et al.  Adjuvant chemotherapy use for Medicare beneficiaries with stage II colon cancer. , 2002, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[70]  K. Abrams,et al.  The risk of colorectal cancer in ulcerative colitis: a meta-analysis , 2001, Gut.

[71]  H. Adami,et al.  Infections as a major preventable cause of human cancer , 2000, Journal of internal medicine.

[72]  S. Bull,et al.  Tumor microsatellite instability and clinical outcome in young patients with colorectal cancer. , 2000, The New England journal of medicine.

[73]  C. Ratto,et al.  Accurate lymph-node detection in colorectal specimens resected for cancer is of prognostic significance , 1999, Diseases of the colon and rectum.

[74]  H Nagura,et al.  CD8+ T cells infiltrated within cancer cell nests as a prognostic factor in human colorectal cancer. , 1998, Cancer research.

[75]  Per Capita,et al.  About the authors , 1995, Machine Vision and Applications.

[76]  A R Feinstein,et al.  The Will Rogers phenomenon. Stage migration and new diagnostic techniques as a source of misleading statistics for survival in cancer. , 1985, The New England journal of medicine.

[77]  A. Jemal,et al.  Cancer statistics, 2012 , 2012, CA: a cancer journal for clinicians.

[78]  M. Kloor,et al.  The localization and density of immune cells in primary tumors of human metastatic colorectal cancer shows an association with response to chemotherapy. , 2009, Cancer immunity.

[79]  P. Loehrer Long-term Use of Aspirin and Nonsteroidal Anti-inflammatory Drugs and Risk of Colorectal Cancer , 2007 .

[80]  R. Blumberg,et al.  The immunology of mucosal models of inflammation. , 2002, Annual review of immunology.

[81]  N. Dubrawsky Cancer statistics , 1989, CA: a cancer journal for clinicians.

[82]  L. Old,et al.  IMMUNOLOGY OF EXPERIMENTAL TUMORS. , 1964, Annual review of medicine.

[83]  Old Lj,et al.  Immunology of Experimental Tumors , 1964 .