Proteogenomic analysis of human colon carcinoma cell lines LIM1215, LIM1899, and LIM2405.

As part of the genome-wide and chromosome-centric human proteomic project (C-HPP), we have integrated shotgun proteomics approach and a genome-wide transcriptomic approach (RNA-Seq) of a set of human colon cancer cell lines (LIM1215, LIM1899 and LIM2405) that were selected to represent a wide range of pathological states of colorectal cancer. The combination of a standard proteomics approach (1D-gel electrophoresis coupled to LC/ion trap mass spectrometry) and RNA-Seq allowed us to exploit the greater depth of the transcriptomics measurement (∼ 9800 transcripts per cell line) versus the protein observations (∼ 1900 protein identifications per cell line). Conversely, the proteomics data were helpful in identifying both cancer associated proteins with differential expression patterns as well as protein networks and pathways which appear to be deregulated in these cell lines. Examples of potential markers include mortalin, nucleophosmin, ezrin, LASP1, alpha and beta forms of spectrin, exportin, the carcinoembryonic antigen family, EGFR and MET. Interaction analyses identified the large intermediate filament family, the protein folding network and adapter proteins in focal adhesion networks, which included the CDC42 and RHOA signaling pathways that may have potential for identifying phenotypic states representing poorly and moderately differentiated states of CRC, with or without metastases.

[1]  A. Scarpa,et al.  Non‐invasive cancer detection: Strategies for the identification of novel cancer markers , 2006, IUBMB life.

[2]  Kaspar Valgepea,et al.  Corrigendum to: “Comparison and applications of label-free absolute proteome quantification methods on Escherichia coli” [J Proteomics 75 (17) (2012) 5437–5448] , 2013 .

[3]  H. Lee,et al.  CEACAM5 and CEACAM6 are major target genes for Smad3-mediated TGF-β signaling , 2008, Oncogene.

[4]  S. Kjellqvist,et al.  A Combined Proteomic and Transcriptomic Approach Shows Diverging Molecular Mechanisms in Thoracic Aortic Aneurysm Development in Patients with Tricuspid- And Bicuspid Aortic Valve* , 2012, Molecular & Cellular Proteomics.

[5]  F. Claessens,et al.  Influence of nucleophosmin/B23 on DNA binding and transcriptional activity of the androgen receptor in prostate cancer cell , 2008, Oncogene.

[6]  J. Rosa,et al.  Proteomic analysis of low‐ to high‐grade astrocytomas reveals an alteration of the expression level of raf kinase inhibitor protein and nucleophosmin , 2010, Proteomics.

[7]  H. Tjalsma Identification of biomarkers for colorectal cancer through proteomics-based approaches , 2010, Expert review of proteomics.

[8]  Jeffrey W. Smith,et al.  Mass Spectrometry-Based Label-Free Quantitative Proteomics , 2009, Journal of biomedicine & biotechnology.

[9]  T. Tuohy,et al.  Hereditary and familial colon cancer. , 2010, Gastroenterology.

[10]  D. Ciocca,et al.  Heat shock proteins in prostate cancer: from tumorigenesis to the clinic , 2010, International journal of hyperthermia : the official journal of European Society for Hyperthermic Oncology, North American Hyperthermia Group.

[11]  E. Marcotte,et al.  Insights into the regulation of protein abundance from proteomic and transcriptomic analyses , 2012, Nature Reviews Genetics.

[12]  C. Haglund,et al.  A retrospective analysis of submissions, acceptance rate, open peer review operations, and prepublication bias of the multidisciplinary open access journal Head & Face Medicine , 2006, PLoS biology.

[13]  E. Reddy,et al.  Transforming growth factor-beta suppresses nonmetastatic colon cancer through Smad4 and adaptor protein ELF at an early stage of tumorigenesis. , 2005, Cancer research.

[14]  M. Gerstein,et al.  RNA-Seq: a revolutionary tool for transcriptomics , 2009, Nature Reviews Genetics.

[15]  S. Le,et al.  Sequence signatures and mRNA concentration can explain two-thirds of protein abundance variation in a human cell line , 2010, Molecular systems biology.

[16]  John Quackenbush,et al.  Synchronous global assessment of gene and protein expression in colorectal cancer progression. , 2005, Genomics.

[17]  A. Sickmann,et al.  Overexpression of LASP-1 mediates migration and proliferation of human ovarian cancer cells and influences zyxin localisation , 2007, British Journal of Cancer.

[18]  J. Yates,et al.  Shotgun Proteomics and Biomarker Discovery , 2002, Disease markers.

[19]  Gary D. Bader,et al.  Pathway Commons, a web resource for biological pathway data , 2010, Nucleic Acids Res..

[20]  Jian-ming Li,et al.  Promotion of colorectal cancer growth and metastasis by the LIM and SH3 domain protein 1 , 2010, Gut.

[21]  Minshan Chen,et al.  Decreased expression of XPO4 is associated with poor prognosis in hepatocellular carcinoma , 2011, Journal of gastroenterology and hepatology.

[22]  M. Gerstein,et al.  The Transcriptional Landscape of the Yeast Genome Defined by RNA Sequencing , 2008, Science.

[23]  Christian von Mering,et al.  STRING 8—a global view on proteins and their functional interactions in 630 organisms , 2008, Nucleic Acids Res..

[24]  C. Caulin,et al.  Oncogenic regulation and function of keratins 8 and 18 , 1996, Cancer and Metastasis Reviews.

[25]  W. Hancock,et al.  Chromosome 7-centric analysis of proteomics data from a panel of human colon carcinoma cell lines. , 2013, Journal of proteome research.

[26]  A. Papavassiliou,et al.  Dual targeting of EGFR and HER-2 in colon cancer cell lines , 2009, Cancer Chemotherapy and Pharmacology.

[27]  Q. Zhang,et al.  High level of ezrin expression in colorectal cancer tissues is closely related to tumor malignancy. , 2009, World journal of gastroenterology.

[28]  K. Resing,et al.  Comparison of Label-free Methods for Quantifying Human Proteins by Shotgun Proteomics*S , 2005, Molecular & Cellular Proteomics.

[29]  K. Syrjänen,et al.  Intense cytoplasmic ezrin immunoreactivity predicts poor survival in colorectal cancer. , 2008, Human pathology.

[30]  E. Lundberg,et al.  A global view of protein expression in human cells, tissues, and organs , 2009, Molecular systems biology.

[31]  Lennart Martens,et al.  The Proteomics Identifications database: 2010 update , 2009, Nucleic Acids Res..

[32]  J. Luk,et al.  Association of Mortalin (HSPA9) with Liver Cancer Metastasis and Prediction for Early Tumor Recurrence* , 2008, Molecular & Cellular Proteomics.

[33]  J. Casal,et al.  Differential protein expression on the cell surface of colorectal cancer cells associated to tumor metastasis , 2010, Proteomics.

[34]  B. Leggett Family‐based screening for colorectal cancer: The Australian perspective , 2009, Journal of gastroenterology and hepatology.

[35]  M. Becich,et al.  Gene expression profiles of prostate cancer reveal involvement of multiple molecular pathways in the metastatic process , 2007, BMC Cancer.

[36]  Tsviya Olender,et al.  Human Gene-Centric Databases at the Weizmann Institute of Science: GeneCards, UDB, CroW 21 and HORDE , 2003, Nucleic Acids Res..

[37]  J. Primrose,et al.  The use of tumour markers CEA, CA-195 and CA-242 in evaluating the response to chemotherapy in patients with advanced colorectal cancer. , 1993, British Journal of Cancer.

[38]  Xiaoyun Fu,et al.  Spectral index for assessment of differential protein expression in shotgun proteomics. , 2008, Journal of proteome research.

[39]  Takahiro Tanaka,et al.  Biomarkers for Colorectal Cancer , 2010, International journal of molecular sciences.

[40]  M. Arpin,et al.  The membrane cytoskeletal crosslinker ezrin is required for metastasis of breast carcinoma cells , 2005, Breast Cancer Research.

[41]  E. Diamandis,et al.  Proteomics Analysis of Conditioned Media from Three Breast Cancer Cell Lines , 2007, Molecular & Cellular Proteomics.

[42]  Joseph J. Pereira,et al.  Proteomic analysis of the human colon carcinoma cell line (LIM 1215): Development of a membrane protein database , 2000, Electrophoresis.

[43]  Moyez Dharsee,et al.  Proteomic Analyses Reveal High Expression of Decorin and Endoplasmin (HSP90B1) Are Associated with Breast Cancer Metastasis and Decreased Survival , 2012, PloS one.

[44]  Robertson Craig,et al.  TANDEM: matching proteins with tandem mass spectra. , 2004, Bioinformatics.

[45]  R. Whitehead,et al.  A colon cancer cell line (LIM1215) derived from a patient with inherited nonpolyposis colorectal cancer. , 1985, Journal of the National Cancer Institute.

[46]  Hong-Jun Yang,et al.  Focal Adhesion Plaque Associated Cytoskeletons Are Involved in the Invasion and Metastasis of Human Colorectal Carcinoma , 2009, Cancer investigation.

[47]  J. Yun,et al.  Increased expression of nucleophosmin/B23 in hepatocellular carcinoma and correlation with clinicopathological parameters , 2007, British Journal of Cancer.

[48]  C. Jilg,et al.  LASP-1, a novel urinary marker for detection of bladder cancer. , 2013, Urologic oncology.

[49]  G. Tell,et al.  Nucleophosmin is overexpressed in thyroid tumors. , 2010, Biochemical and biophysical research communications.

[50]  J. Yates,et al.  A model for random sampling and estimation of relative protein abundance in shotgun proteomics. , 2004, Analytical chemistry.

[51]  F. Barany,et al.  c-Met gene amplification is associated with advanced stage colorectal cancer and liver metastases. , 2008, Cancer letters.

[52]  Robin P Boushey,et al.  Colorectal cancer epidemiology: incidence, mortality, survival, and risk factors. , 2009, Clinics in colon and rectal surgery.

[53]  S. Hanash,et al.  A chromosome-centric human proteome project (C-HPP) to characterize the sets of proteins encoded in chromosome 17. , 2013, Journal of proteome research.

[54]  R. Johnstone,et al.  Tumor localization by combinations of monoclonal antibodies in a new human colon carcinoma cell line (LIM1899). , 1990, Cancer research.

[55]  Pedro Larrañaga,et al.  Identification of a biomarker panel for colorectal cancer diagnosis , 2012, BMC Cancer.

[56]  Qiang Zhang,et al.  Ezrin promotes invasion and metastasis of pancreatic cancer cells , 2010, Journal of Translational Medicine.

[57]  R. Whitehead,et al.  Retention of tissue‐specific phenotype in a panel of colon carcinoma cell lines: Relationship to correlates , 1992 .

[58]  A. Chevinsky CEA in tumors of other than colorectal origin. , 1991, Seminars in surgical oncology.

[59]  M. MacCoss,et al.  Shotgun proteomics: tools for the analysis of complex biological systems. , 2002, Current opinion in molecular therapeutics.

[60]  G. Murray,et al.  Mortalin is over‐expressed by colorectal adenocarcinomas and correlates with poor survival , 2005, The Journal of pathology.

[61]  Michael P. Snyder,et al.  RNA‐Seq: A Method for Comprehensive Transcriptome Analysis , 2010, Current protocols in molecular biology.

[62]  Frank Staib,et al.  Genetics of hepatocellular carcinoma. , 2007, World journal of gastroenterology.

[63]  Knut Reinert,et al.  Tools for Label-free Peptide Quantification , 2012, Molecular & Cellular Proteomics.

[64]  Brad T. Sherman,et al.  DAVID: Database for Annotation, Visualization, and Integrated Discovery , 2003, Genome Biology.

[65]  S. Fukushima,et al.  Cytokeratin 8/18 overexpression and complex formation as an indicator of GST-P positive foci transformation into hepatocellular carcinomas , 2009, Toxicology and Applied Pharmacology.

[66]  Joshua E. Elias,et al.  Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: the yeast proteome. , 2003, Journal of proteome research.

[67]  Michael K. Coleman,et al.  Correlation of relative abundance ratios derived from peptide ion chromatograms and spectrum counting for quantitative proteomic analysis using stable isotope labeling. , 2005, Analytical chemistry.

[68]  Sonja Gillen,et al.  Reduced expression of the membrane skeleton protein beta1-spectrin (SPTBN1) is associated with worsened prognosis in pancreatic cancer. , 2010, Histology and histopathology.

[69]  Rosamonde E Banks,et al.  Housekeeping proteins: A preliminary study illustrating some limitations as useful references in protein expression studies , 2005, Proteomics.

[70]  W. Hancock,et al.  Approaches to the study of N-linked glycoproteins in human plasma using lectin affinity chromatography and nano-HPLC coupled to electrospray linear ion trap--Fourier transform mass spectrometry. , 2006, Glycobiology.

[71]  T. G. Grunewald,et al.  The LIM and SH3 domain protein family: structural proteins or signal transducers or both? , 2008, Molecular Cancer.

[72]  M. Gilcrease,et al.  Integrin signaling in epithelial cells. , 2007, Cancer letters.

[73]  J. Yates,et al.  The application of mass spectrometry to membrane proteomics , 2003, Nature Biotechnology.

[74]  J. Weinstein,et al.  Biomarkers in Cancer Staging, Prognosis and Treatment Selection , 2005, Nature Reviews Cancer.

[75]  K. Valgepea,et al.  Comparison and applications of label-free absolute proteome quantification methods on Escherichia coli. , 2012, Journal of proteomics.

[76]  M. Imieliński,et al.  Integrated Proteomic, Transcriptomic, and Biological Network Analysis of Breast Carcinoma Reveals Molecular Features of Tumorigenesis and Clinical Relapse* , 2012, Molecular & Cellular Proteomics.

[77]  D. Schriemer,et al.  Integration of deep transcriptome and proteome analyses reveals the components of alkaloid metabolism in opium poppy cell cultures , 2010, BMC Plant Biology.

[78]  M. Mann,et al.  Defining the transcriptome and proteome in three functionally different human cell lines , 2010, Molecular systems biology.

[79]  B. Têtu,et al.  Gene expression profiling of paired ovarian tumors obtained prior to and following adjuvant chemotherapy: molecular signatures of chemoresistant tumors. , 2006, International journal of oncology.

[80]  Jie Zheng,et al.  [Study of genes related to gastric cancer and its premalignant lesions with fluorescent differential display]. , 2004, Ai zheng = Aizheng = Chinese journal of cancer.