CDX2 as a Prognostic Biomarker in Stage II and Stage III Colon Cancer.

Background The identification of high-risk stage II colon cancers is key to the selection of patients who require adjuvant treatment after surgery. Microarray-based multigene-expression signatures derived from stem cells and progenitor cells hold promise, but they are difficult to use in clinical practice. Methods We used a new bioinformatics approach to search for biomarkers of colon epithelial differentiation across gene-expression arrays and then ranked candidate genes according to the availability of clinical-grade diagnostic assays. With the use of subgroup analysis involving independent and retrospective cohorts of patients with stage II or stage III colon cancer, the top candidate gene was tested for its association with disease-free survival and a benefit from adjuvant chemotherapy. Results The transcription factor CDX2 ranked first in our screening test. A group of 87 of 2115 tumor samples (4.1%) lacked CDX2 expression. In the discovery data set, which included 466 patients, the rate of 5-year disease-free survival was lower among the 32 patients (6.9%) with CDX2-negative colon cancers than among the 434 (93.1%) with CDX2-positive colon cancers (hazard ratio for disease recurrence, 3.44; 95% confidence interval [CI], 1.60 to 7.38; P=0.002). In the validation data set, which included 314 patients, the rate of 5-year disease-free survival was lower among the 38 patients (12.1%) with CDX2 protein-negative colon cancers than among the 276 (87.9%) with CDX2 protein-positive colon cancers (hazard ratio, 2.42; 95% CI, 1.36 to 4.29; P=0.003). In both these groups, these findings were independent of the patient's age, sex, and tumor stage and grade. Among patients with stage II cancer, the difference in 5-year disease-free survival was significant both in the discovery data set (49% among 15 patients with CDX2-negative tumors vs. 87% among 191 patients with CDX2-positive tumors, P=0.003) and in the validation data set (51% among 15 patients with CDX2-negative tumors vs. 80% among 106 patients with CDX2-positive tumors, P=0.004). In a pooled database of all patient cohorts, the rate of 5-year disease-free survival was higher among 23 patients with stage II CDX2-negative tumors who were treated with adjuvant chemotherapy than among 25 who were not treated with adjuvant chemotherapy (91% vs. 56%, P=0.006). Conclusions Lack of CDX2 expression identified a subgroup of patients with high-risk stage II colon cancer who appeared to benefit from adjuvant chemotherapy. (Funded by the National Comprehensive Cancer Network, the National Institutes of Health, and others.).

[1]  H. Stein,et al.  Molecular profiles and clinical outcome of stage UICC II colon cancer patients , 2011, International Journal of Colorectal Disease.

[2]  Robert Tibshirani,et al.  Boolean implication networks derived from large scale, whole genome microarray datasets , 2008, Genome Biology.

[3]  K. Chawengsaksophak,et al.  Homeosis and intestinal tumours in Cdx2 mutant mice , 1997, Nature.

[4]  T. Hickish,et al.  Oxaliplatin, fluorouracil, and leucovorin as adjuvant treatment for colon cancer. , 2004, The New England journal of medicine.

[5]  L. Kirkeby,et al.  Gene expression profiles in stages II and III colon cancers: application of a 128-gene signature , 2012, International Journal of Colorectal Disease.

[6]  Florian Markowetz,et al.  Poor-prognosis colon cancer is defined by a molecularly distinct subtype and develops from serrated precursor lesions , 2013, Nature Medicine.

[7]  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.

[8]  Shuji Ogino,et al.  Relationship of CDX2 Loss with Molecular Features and Prognosis in Colorectal Cancer , 2009, Clinical Cancer Research.

[9]  E. J. Stringer,et al.  The role of Cdx genes in the gut and in axial development. , 2010, Biochemical Society transactions.

[10]  N. Cho,et al.  Loss of CDX2 expression is associated with poor prognosis in colorectal cancer patients. , 2015, World journal of gastroenterology.

[11]  M. Wong,et al.  Characterization of the intestinal cancer stem cell marker CD166 in the human and mouse gastrointestinal tract. , 2010, Gastroenterology.

[12]  Carolyn Compton,et al.  American Joint Committee on Cancer prognostic factors consensus conference , 2000, Cancer.

[13]  T. Yeatman,et al.  Experimentally derived metastasis gene expression profile predicts recurrence and death in patients with colon cancer. , 2010, Gastroenterology.

[14]  A. Gown,et al.  CDX2, a Highly Sensitive and Specific Marker of Adenocarcinomas of Intestinal Origin: An Immunohistochemical Survey of 476 Primary and Metastatic Carcinomas , 2003, The American journal of surgical pathology.

[15]  N. Meropol Ongoing challenge of stage II colon cancer. , 2011, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[16]  David C. Atkins,et al.  Gene expression profiles and molecular markers to predict recurrence of Dukes' B colon cancer. , 2004, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[17]  Hans Clevers,et al.  The intestinal stem cell signature identifies colorectal cancer stem cells and predicts disease relapse. , 2011, Cell stem cell.

[18]  Kathleen R. Cho,et al.  Loss of CDX2 expression and microsatellite instability are prominent features of large cell minimally differentiated carcinomas of the colon. , 2001, The American journal of pathology.

[19]  C. Tournigand,et al.  Chemotherapy: Is adjuvant chemotherapy an option for stage II colon cancer? , 2011, Nature Reviews Clinical Oncology.

[20]  M Dietel,et al.  ALCAM/CD166 is overexpressed in colorectal carcinoma and correlates with shortened patient survival , 2004, Journal of Clinical Pathology.

[21]  S. Dudoit,et al.  Stage II colon cancer prognosis prediction by tumor gene expression profiling. , 2006, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[22]  G. Sherlock,et al.  The prognostic role of a gene signature from tumorigenic breast-cancer cells. , 2007, The New England journal of medicine.

[23]  J. Efron,et al.  Dilemma of stage II colon cancer and decision making for adjuvant chemotherapy. , 2014, Journal of the American College of Surgeons.

[24]  L. Terracciano,et al.  Differential diagnostic and functional role of the multi-marker phenotype CDX2/CK20/CK7 in colorectal cancer stratified by mismatch repair status , 2008, Modern Pathology.

[25]  T. Ørntoft,et al.  Metastasis-Associated Gene Expression Changes Predict Poor Outcomes in Patients with Dukes Stage B and C Colorectal Cancer , 2009, Clinical Cancer Research.

[26]  A. Folpe,et al.  CDX-2, a New Marker for Adenocarcinoma of Gastrointestinal Origin , 2004, Advances in anatomic pathology.

[27]  Debashis Sahoo,et al.  Extracting binary signals from microarray time-course data , 2007, Nucleic acids research.

[28]  M. Vyberg,et al.  Demonstration of CDX2 is Highly Antibody Dependant , 2012, Applied immunohistochemistry & molecular morphology : AIMM.

[29]  D. Birnbaum,et al.  A seven-gene signature aggregates a subgroup of stage II colon cancers with stage III. , 2012, Omics : a journal of integrative biology.

[30]  L. Terracciano,et al.  Combined analysis of specific KRAS mutation, BRAF and microsatellite instability identifies prognostic subgroups of sporadic and hereditary colorectal cancer , 2010, International journal of cancer.

[31]  L. Terracciano,et al.  Clinicopathological and protein characterization of BRAF‐ and K‐RAS‐mutated colorectal cancer and implications for prognosis , 2010, International journal of cancer.

[32]  D. Jäger,et al.  [Systemic therapy for colorectal cancer]. , 2005, Der Chirurg; Zeitschrift fur alle Gebiete der operativen Medizen.

[33]  S. Cha,et al.  Pooled analysis of fluorouracil-based adjuvant therapy for stage II and III colon cancer: who benefits and by how much? , 2004, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[34]  Margarita Lopatin,et al.  Validation of the 12-gene colon cancer recurrence score in NSABP C-07 as a predictor of recurrence in patients with stage II and III colon cancer treated with fluorouracil and leucovorin (FU/LV) and FU/LV plus oxaliplatin. , 2013, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[35]  Pradeep S Rajendran,et al.  Single-cell dissection of transcriptional heterogeneity in human colon tumors , 2011, Nature Biotechnology.

[36]  D. Sargent,et al.  Adjuvant chemotherapy for resected stage II and III colon cancer: comparison of two widely used prognostic calculators. , 2010, Seminars in oncology.

[37]  J P Pignon,et al.  Irinotecan plus fluorouracil and leucovorin for metastatic colorectal cancer. , 2001, The New England journal of medicine.

[38]  M. Loda,et al.  The homeobox intestinal differentiation factor CDX2 is selectively expressed in gastrointestinal adenocarcinomas , 2004, Modern Pathology.

[39]  Michael F. Clarke,et al.  Phenotypic characterization of human colorectal cancer stem cells , 2007, Proceedings of the National Academy of Sciences.