Aberrant crypt foci as precursors in colorectal cancer progression

Colorectal cancer progression originates when accumulated genetic and epigenetic alterations cause genomic instability and a malignant phenotype. Subsequent molecular pathway deregulation leads to histopathologic changes that are clinically evident as aberrant crypt foci (ACF) and visualized by high‐magnification chromoscopic colonoscopy. ACF are biomarkers of increased colorectal cancer risk, particularly those with dysplastic features. Genetic profiling using genomic instability, loss of heterozygosity, and methylation analysis has revealed a minority population of ACF genotypically analogous to cancer. J. Surg. Oncol. 2008;98:207–213. © 2008 Wiley‐Liss, Inc.

[1]  S. Baylin,et al.  Identification of differentially methylated sequences in colorectal cancer by methylated CpG island amplification. , 1999, Cancer research.

[2]  Y. Nakamura,et al.  Allelotype of colorectal carcinomas. , 1989, Science.

[3]  Minjin Lee,et al.  Prognostic value of p16INK4a and p14ARF gene hypermethylation in human colon cancer. , 2006, Pathology, research and practice.

[4]  Jeffrey S. Morris,et al.  Concordant CpG island methylation in hyperplastic polyposis. , 2002, The American journal of pathology.

[5]  D. Stoler,et al.  Cancer: the evolved consequence of a destabilized genome , 2001, BioEssays : news and reviews in molecular, cellular and developmental biology.

[6]  L. Roncucci,et al.  Microsatellite instability and mismatch-repair protein expression in hereditary and sporadic colorectal carcinogenesis. , 2001, Cancer research.

[7]  S. Schwartz,et al.  The identification of monoclonality in human aberrant crypt foci. , 1999, Cancer research.

[8]  H. Esumi,et al.  Frequent and characteristic K-ras activation and absence of p53 protein accumulation in aberrant crypt foci of the colon. , 1995, Gastroenterology.

[9]  M. Nucci,et al.  Phenotypic and genotypic characteristics of aberrant crypt foci in human colorectal mucosa. , 1997, Human pathology.

[10]  P. Nambiar,et al.  Differential Expression of p16INK4a in Azoxymethane‐Induced Mouse Colon Tumorigenesis , 2000, Molecular carcinogenesis.

[11]  T. Muto,et al.  The evolution of cancer of the colon and rectum , 1975, Cancer.

[12]  W. Willett.  The search for the causes of breast and colon cancer , 1989, Nature.

[13]  F. Bosman,et al.  Aberrant crypt foci in patients with neoplastic and nonneoplastic colonic disease. , 1999, Human pathology.

[14]  Wei Dong Chen,et al.  Epigenetic inactivation of SFRP genes allows constitutive WNT signaling in colorectal cancer , 2004, Nature Genetics.

[15]  Christopher D. Heinen,et al.  Microsatellite instability in aberrant crypt foci from human colons. , 1996, Cancer research.

[16]  Junji Kato,et al.  Aberrant Crypt Foci of the Colon as Precursors of Adenoma and Cancer , 1998 .

[17]  R P Bird,et al.  Observation and quantification of aberrant crypts in the murine colon treated with a colon carcinogen: preliminary findings. , 1987, Cancer letters.

[18]  J. Bernheim,et al.  Aberrant crypt foci in human colons: distribution and histomorphologic characteristics. , 1998, Human pathology.

[19]  I. Johnson.  Phytochemicals and cancer , 2007, Proceedings of the Nutrition Society.

[20]  J. Faivre,et al.  Adenoma‐carcinoma sequence or “de novo” Carcinogenesis?. A study of adenomatous remnants in a population‐based series of large bowel cancers , 1992, Cancer.

[21]  Carol R Regueiro,et al.  AGA Future Trends Committee report: Colorectal cancer: a qualitative review of emerging screening and diagnostic technologies. , 2005, Gastroenterology.

[22]  B. Morson.  Precancerous and early malignant lesions of the large intestine , 1968, The British journal of surgery.

[23]  S. Kuramoto,et al.  How do colorectal cancers develop? , 1995, Cancer.

[24]  L. Roncucci,et al.  Identification and quantification of aberrant crypt foci and microadenomas in the human colon. , 1991, Human pathology.

[25]  T. Takayama,et al.  Aberrant Crypt Foci as Precursors of the Dysplasia-Carcinoma Sequence in Patients with Ulcerative Colitis , 2008, Clinical Cancer Research.

[26]  M. Loda,et al.  Methylation of the hMLH1 promoter correlates with lack of expression of hMLH1 in sporadic colon tumors and mismatch repair-defective human tumor cell lines. , 1997, Cancer research.

[27]  S. Yoshida,et al.  Detection of aberrant crypt foci by magnifying colonoscopy , 1995 .

[28]  D. P. Hurlstone,et al.  Practical uses of chromoendoscopy and magnification at colonoscopy. , 2005, Gastrointestinal endoscopy clinics of North America.

[29]  E. Kaplan,et al.  K-ras mutations in putative preneoplastic lesions in human colon. , 1993, Journal of the National Cancer Institute.

[30]  A. Gartel,et al.  Myc-ARF (Alternate Reading Frame) Interaction Inhibits the Functions of Myc* , 2004, Journal of Biological Chemistry.

[31]  T. Smyrk,et al.  Flat cancers do develop in the polyp-free large intestine , 1997 .

[32]  W. Kaelin,et al.  Role of the retinoblastoma protein in the pathogenesis of human cancer. , 1997, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[33]  Junji Kato,et al.  Aberrant crypt foci of the colon as precursors of adenoma and cancer , 1998, The New England journal of medicine.

[34]  N. Ahuja,et al.  Distinct genetic profiles in colorectal tumors with or without the CpG island methylator phenotype. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[35]  N. Petrelli,et al.  Allelic losses at genomic instability-associated loci in villous adenomas and adjacent colorectal cancers. , 2007, Cancer genetics and cytogenetics.

[36]  H. Esumi,et al.  Emergence of adenomatous aberrant crypt foci (ACF) from hyperplastic ACF with concomitant increase in cell proliferation. , 1995, Cancer research.

[37]  S. Finkelstein,et al.  K-ras and p53 mutations in aberrant crypt foci and colonic tumors from colon cancer patients. , 1997, Cancer letters.

[38]  N. Nowak,et al.  Intrachromosomal genomic instability in human sporadic colorectal cancer measured by genome-wide allelotyping and inter-(simple sequence repeat) PCR. , 2001, Cancer research.

[39]  J. Bernheim,et al.  Proliferating cell nuclear antigen as a marker of cell kinetics in aberrant crypt foci, hyperplastic polyps, adenomas, and adenocarcinomas of the human colon. , 1997, American journal of surgery.

[40]  J. Meyerhardt,et al.  Correlation of beta-catenin localization with cyclooxygenase-2 expression and CpG island methylator phenotype (CIMP) in colorectal cancer. , 2007, Neoplasia.

[41]  M. Toyota,et al.  Aberrant methylation of the Cyclooxygenase 2 CpG island in colorectal tumors. , 2000, Cancer research.

[42]  L. Roncucci,et al.  Classification of aberrant crypt foci and microadenomas in human colon. , 1991, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[43]  T. Takayama,et al.  Analysis of K-ras, APC, and beta-catenin in aberrant crypt foci in sporadic adenoma, cancer, and familial adenomatous polyposis. , 2001, Gastroenterology.

[44]  R. Wolff,et al.  Evaluation of a large, population-based sample supports a CpG island methylator phenotype in colon cancer. , 2005, Gastroenterology.

[45]  N. Petrelli,et al.  Genomic heterogeneity and instability in colorectal cancer: spectral karyotyping, glutathione transferase-Ml and ras. , 2004, Mutation research.

[46]  Martin Werner,et al.  Array CGH identifies distinct DNA copy number profiles of oncogenes and tumor suppressor genes in chromosomal- and microsatellite-unstable sporadic colorectal carcinomas , 2007, Journal of Molecular Medicine.

[47]  P. Rauch,et al.  Human p14ARF-mediated cell cycle arrest strictly depends on intact p53 signaling pathways , 2002, Oncogene.

[48]  E. Furth,et al.  p16(INK4a) expression begins early in human colon neoplasia and correlates inversely with markers of cell proliferation. , 2000, Gastroenterology.

[49]  W. Haenszel,et al.  Large-bowel cancer in Hawaiian Japanese. , 1973, Journal of the National Cancer Institute.

[50]  I. Johnson.  New approaches to the role of diet in the prevention of cancers of the alimentary tract. , 2004, Mutation research.

[51]  D. Present,et al.  Consensus conference: Colorectal cancer screening and surveillance in inflammatory bowel disease. , 2005, Inflammatory bowel diseases.

[52]  T. P. Pretlow,et al.  DNA alterations in human aberrant crypt foci and colon cancers by random primed polymerase chain reaction. , 2003, Cancer research.

[53]  E. Fearon,et al.  Role of the dependence receptor DCC in colorectal cancer pathogenesis. , 2004, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[54]  C. Plass,et al.  SLC5A8, a sodium transporter, is a tumor suppressor gene silenced by methylation in human colon aberrant crypt foci and cancers , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[55]  Jeffrey S. Morris,et al.  BRAF mutations in aberrant crypt foci and hyperplastic polyposis. , 2005, The American journal of pathology.

[56]  I. Siu,et al.  Identification of dysplasia in human colonic aberrant crypt foci. , 1997, The American journal of pathology.

[57]  R. Schneider-Stock,et al.  Differences in loss of p16INK4 protein expression by promoter methylation between left- and right-sided primary colorectal carcinomas. , 2003, International Journal of Oncology.

[58]  N. Nowak,et al.  Genomic instability of human aberrant crypt foci measured by inter-(simple sequence repeat) PCR and array-CGH. , 2006, Mutation research.

[59]  A. Zauber,et al.  Prevention of colorectal cancer by colonoscopic polypectomy. The National Polyp Study Workgroup. , 1993 .

[60]  M. Monden,et al.  Methylation and expression of p16INK4 tumor suppressor gene in primary colorectal cancer tissues. , 2005, International journal of oncology.

[61]  A. Medline,et al.  Dose response and proliferative characteristics of aberrant crypt foci: putative preneoplastic lesions in rat colon. , 1991, Carcinogenesis.

[62]  S. Gallinger,et al.  Somatic APC and K-ras codon 12 mutations in aberrant crypt foci from human colons. , 1994, Cancer research.

[63]  T. Sugimura,et al.  Altered expression of beta-catenin, inducible nitric oxide synthase and cyclooxygenase-2 in azoxymethane-induced rat colon carcinogenesis. , 2000, Carcinogenesis.

[64]  Xiao-Jun Ma,et al.  Genetic signatures of High- and Low-Risk Aberrant Crypt Foci in a Mouse Model of Sporadic Colon Cancer , 2004, Cancer Research.

[65]  E. Giovannucci.  An updated review of the epidemiological evidence that cigarette smoking increases risk of colorectal cancer. , 2001, Cancer epidemiology, biomarkers & prevention : a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology.

[66]  B. Amati,et al.  Cyclin E and c‐Myc promote cell proliferation in the presence of p16INK4a and of hypophosphorylated retinoblastoma family proteins , 1997, The EMBO journal.

[67]  D. Kristt,et al.  Colonic aberrant crypts may originate from impaired fissioning: relevance to increased risk of neoplasia. , 1999, Human pathology.

[68]  J. Bernheim,et al.  Chemopreventive effect of aspirin on growth of aberrant crypt foci in rats , 1998, International Journal of Colorectal Disease.

[69]  J. Mason,et al.  Relationship of aging and tobacco use with the development of aberrant crypt foci in a predominantly African-American population. , 2005, Clinical gastroenterology and hepatology : the official clinical practice journal of the American Gastroenterological Association.

[70]  N. Petrelli,et al.  The onset and extent of genomic instability in sporadic colorectal tumor progression. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[71]  C. Rao,et al.  Chemopreventive properties of a selective inducible nitric oxide synthase inhibitor in colon carcinogenesis, administered alone or in combination with celecoxib, a selective cyclooxygenase-2 inhibitor. , 2002, Cancer research.

[72]  J. Herman,et al.  CpG island methylator phenotype in colorectal cancer. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[73]  F. Sinicrope,et al.  Expression of Cellular Adhesion Proteins and Abnormal Glycoproteins in Human Aberrant Crypt Foci , 2004, Applied immunohistochemistry & molecular morphology : AIMM.

[74]  Wei-Dong Chen,et al.  CpG island methylation in aberrant crypt foci and cancers from the same patients , 2005, International journal of cancer.

[75]  J. Issa,et al.  CpG island methylation in aberrant crypt foci of the colorectum. , 2002, The American journal of pathology.

[76]  L. Roncucci,et al.  Histology of aberrant crypt foci in the human colon , 1997, Histopathology.

[77]  H. Esumi,et al.  Instability of X chromosome methylation in aberrant crypt foci of the human colon. , 2000, Cancer research.

[78]  S. Cross,et al.  Further validation of high-magnification chromoscopic-colonoscopy for the detection of intraepithelial neoplasia and colon cancer in ulcerative colitis. , 2004, Gastroenterology.

[79]  V. Villanacci,et al.  Aberrant crypt foci in the human colon: frequency and histologic patterns in patients with colorectal cancer or diverticular disease. , 1999, The American journal of surgical pathology.

[80]  K. Hatakeyama,et al.  Aberrant expression of pRb and p16(INK4), alone or in combination, indicates poor outcome after resection in patients with colorectal carcinoma. , 2004, Human pathology.

[81]  S. Kudo,et al.  Diagnosis of colorectal tumorous lesions by magnifying endoscopy. , 1996, Gastrointestinal endoscopy.

[82]  N. Petrelli,et al.  Genomic instability in sporadic colorectal cancer quantitated by inter‐simple sequence repeat PCR analysis , 1997, Genes, chromosomes & cancer.

[83]  B. Levin,et al.  Cigarette smoking and alcohol consumption as risk factors for colorectal adenomatous polyps. , 1995, Journal of the National Cancer Institute.

[84]  J. Herman,et al.  Inactivation of the CDKN2/p16/MTS1 gene is frequently associated with aberrant DNA methylation in all common human cancers. , 1995, Cancer research.

[85]  R. Bird,et al.  Aberrant crypts: potential preneoplastic lesions in the murine colon. , 1988, Cancer research.

[86]  R. Coffey,et al.  Up-regulation of cyclooxygenase 2 gene expression in human colorectal adenomas and adenocarcinomas. , 1994, Gastroenterology.

[87]  Shinji Tanaka,et al.  Nonpolypoid (flat and depressed) colorectal neoplasms. , 2006, Gastroenterology.

[88]  J. Jass,et al.  Clinical importance of DNA content in rectal cancer measured by flow cytometry. , 1989, Journal of clinical pathology.

[89]  T. P. Pretlow,et al.  Aberrant crypts: putative preneoplastic foci in human colonic mucosa. , 1991, Cancer research.

[90]  K. Kinzler,et al.  Molecular determinants of dysplasia in colorectal lesions. , 1994, Cancer research.

[91]  Jeffrey S. Morris,et al.  CpG island methylation in colorectal adenomas. , 2001, The American journal of pathology.

[92]  S N Thibodeau,et al.  Hypermethylation of the hMLH1 promoter in colon cancer with microsatellite instability. , 1998, Cancer research.

[93]  Markus F Neurath,et al.  Chromoendoscopy and other novel imaging techniques. , 2006, Gastroenterology clinics of North America.

[94]  N. Petrelli,et al.  aCGH local copy number aberrations associated with overall copy number genomic instability in colorectal cancer: coordinate involvement of the regions including BCR and ABL. , 2007, Mutation research.

[95]  P. Laird,et al.  CpG island methylator phenotype underlies sporadic microsatellite instability and is tightly associated with BRAF mutation in colorectal cancer , 2006, Nature Genetics.

[96]  Aberrant crypt foci in human colon carcinogenesis. , 1997, Cancer detection and prevention.

[97]  Syed G. Shah,et al.  Total colonic dye-spray increases the detection of diminutive adenomas during routine colonoscopy: a randomized controlled trial. , 2002, Gastrointestinal endoscopy.

[98]  K. Wakabayashi,et al.  Gene mutations and altered gene expression in azoxymethane‐induced colon carcinogenesis in rodents , 2004, Cancer science.

[99]  N. Shivapurkar,et al.  Dietary fiber and the chemopreventive modelation of colon carcinogenesis. , 1996, Mutation research.