Relationship of gene expression and chromosomal abnormalities in colorectal cancer.

Several studies have verified the existence of multiple chromosomal abnormalities in colon cancer. However, the relationships between DNA copy number and gene expression have not been adequately explored nor globally monitored during the progression of the disease. In this work, three types of array-generated data (expression, single nucleotide polymorphism, and comparative genomic hybridization) were collected from a large set of colon cancer patients at various stages of the disease. Probes were annotated to specific chromosomal locations and coordinated alterations in DNA copy number and transcription levels were revealed at specific positions. We show that across many large regions of the genome, changes in expression level are correlated with alterations in DNA content. Often, large chromosomal segments, containing multiple genes, are transcriptionally affected in a coordinated way, and we show that the underlying mechanism is a corresponding change in DNA content. This implies that whereas specific chromosomal abnormalities may arise stochastically, the associated changes in expression of some or all of the affected genes are responsible for selecting cells bearing these abnormalities for clonal expansion. Indeed, particular chromosomal regions are frequently gained and overexpressed (e.g., 7p, 8q, 13q, and 20q) or lost and underexpressed (e.g., 1p, 4, 5q, 8p, 14q, 15q, and 18) in primary colon tumors, making it likely that these changes favor tumorigenicity. Furthermore, we show that these aberrations are absent in normal colon mucosa, appear in benign adenomas (albeit only in a small fraction of the samples), become more frequent as disease advances, and are found in the majority of metastatic samples.

[1]  H. Varmus,et al.  Homogeneously staining chromosomal regions contain amplified copies of an abundantly expressed cellular oncogene (c-myc) in malignant neuroendocrine cells from a human colon carcinoma. , 1983, Proceedings of the National Academy of Sciences of the United States of America.

[2]  E Soeda,et al.  Amplification and overexpression of TGIF2, a novel homeobox gene of the TALE superclass, in ovarian cancer cell lines. , 2000, Biochemical and biophysical research communications.

[3]  Keith W. Jones,et al.  Whole genome DNA copy number changes identified by high density oligonucleotide arrays , 2004, Human Genomics.

[4]  Keith Wilson,et al.  Silence of chromosomal amplifications in colon cancer. , 2002, Cancer research.

[5]  D. Albertson,et al.  Chromosome aberrations in solid tumors , 2003, Nature Genetics.

[6]  T. Ørntoft,et al.  Gene expression in colorectal cancer. , 2002, Cancer research.

[7]  Thomas Ried,et al.  Comparative genomic hybridization reveals a specific pattern of chromosomal gains and losses during the genesis of colorectal tumors , 1996, Genes, chromosomes & cancer.

[8]  Joe W. Gray,et al.  Genome Amplification of Chromosome 20 in Breast Cancer , 2003, Breast Cancer Research and Treatment.

[9]  V. Reuter,et al.  Chromosomal amplification is associated with cisplatin resistance of human male germ cell tumors. , 1998, Cancer research.

[10]  M. Ringnér,et al.  Impact of DNA amplification on gene expression patterns in breast cancer. , 2002, Cancer research.

[11]  X. Guan,et al.  Recurrent genetic alterations in 26 colorectal carcinomas and 21 adenomas from Chinese patients. , 2003, Cancer genetics and cytogenetics.

[12]  W. Linehan,et al.  The consequences of chromosomal aneuploidy on gene expression profiles in a cell line model for prostate carcinogenesis. , 2001, Cancer research.

[13]  I Tomlinson,et al.  APC mutations are sufficient for the growth of early colorectal adenomas. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[14]  John Calvin Reed,et al.  Elevated expression of Bcl-X and reduced Bak in primary colorectal adenocarcinomas. , 1996, Cancer research.

[15]  Dan Tsafrir,et al.  Sorting points into neighborhoods (SPIN): data analysis and visualization by ordering distance matrices , 2005, Bioinform..

[16]  Jane Fridlyand,et al.  High-resolution analysis of DNA copy number alterations in colorectal cancer by array-based comparative genomic hybridization. , 2004, Carcinogenesis.

[17]  K. Dykema,et al.  Comparison of array-based comparative genomic hybridization with gene expression-based regional expression biases to identify genetic abnormalities in hepatocellular carcinoma , 2005, BMC Genomics.

[18]  K. Kinzler,et al.  Cancer genes and the pathways they control , 2004, Nature Medicine.

[19]  Jonathan Pevsner,et al.  Gene expression alterations over large chromosomal regions in cancers include multiple genes unrelated to malignant progression. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[20]  P. Duesberg,et al.  Are cancers dependent on oncogenes or on aneuploidy? , 2003, Cancer genetics and cytogenetics.

[21]  S. Goodman,et al.  Evidence that genetic instability occurs at an early stage of colorectal tumorigenesis. , 2001, Cancer research.

[22]  G. Getz,et al.  Expression profiles of acute lymphoblastic and myeloblastic leukemias with ALL-1 rearrangements , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[23]  N. Carter,et al.  Array Comparative Genomic Hybridization Analysis of Colorectal Cancer Cell Lines and Primary Carcinomas , 2004, Cancer Research.

[24]  Hongyue Dai,et al.  Widespread aneuploidy revealed by DNA microarray expression profiling , 2000, Nature Genetics.

[25]  N. Carter,et al.  DNA microarrays for comparative genomic hybridization based on DOP‐PCR amplification of BAC and PAC clones , 2003, Genes, chromosomes & cancer.

[26]  Christian A. Rees,et al.  Microarray analysis reveals a major direct role of DNA copy number alteration in the transcriptional program of human breast tumors , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[27]  K. Furge,et al.  Identification of frequent cytogenetic aberrations in hepatocellular carcinoma using gene-expression microarray data , 2002, Genome Biology.

[28]  W. Hahn,et al.  Derivation of human tumor cells in vitro without widespread genomic instability. , 2001, Cancer research.

[29]  P. Duesberg,et al.  Aneuploidy vs. gene mutation hypothesis of cancer: recent study claims mutation but is found to support aneuploidy. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[30]  Jean Marx,et al.  Debate Surges Over the Origins of Genomic Defects in Cancer , 2002, Science.