An informatics-assisted label-free approach for personalized tissue membrane proteomics: case study on colorectal cancer

Mol Cell Proteomics. 2011 Apr;10(4):M110.003087. doi: 10.1074/mcp.M110.003087. Epub 2011 Jan 5.

Abstract

We developed a multiplexed label-free quantification strategy, which integrates an efficient gel-assisted digestion protocol, high-performance liquid chromatography tandem MS analysis, and a bioinformatics alignment method to determine personalized proteomic profiles for membrane proteins in human tissues. This strategy provided accurate (6% error) and reproducible (34% relative S.D.) quantification of three independently purified membrane fractions from the same human colorectal cancer (CRC) tissue. Using CRC as a model, we constructed the personalized membrane protein atlas of paired tumor and adjacent normal tissues from 28 patients with different stages of CRC. Without fractionation, this strategy confidently quantified 856 proteins (≥2 unique peptides) across different patients, including the first and robust detection (Mascot score: 22,074) of the well-documented CRC marker, carcinoembryonic antigen 5 by a discovery-type proteomics approach. Further validation of a panel of proteins, annexin A4, neutrophils defensin A1, and claudin 3, confirmed differential expression levels and high occurrences (48-70%) in 60 CRC patients. The most significant discovery is the overexpression of stomatin-like 2 (STOML2) for early diagnostic and prognostic potential. Increased expression of STOML2 was associated with decreased CRC-related survival; the mean survival period was 34.77 ± 2.03 months in patients with high STOML2 expression, whereas 53.67 ± 3.46 months was obtained for patients with low STOML2 expression. Further analysis by ELISA verified that plasma concentrations of STOML2 in early-stage CRC patients were elevated as compared with those of healthy individuals (p < 0.001), suggesting that STOML2 may be a noninvasive serological biomarker for early CRC diagnosis. The overall sensitivity of STOML2 for CRC detection was 71%, which increased to 87% when combined with CEA measurements. This study demonstrated a sensitive, label-free strategy for differential analysis of tissue membrane proteome, which may provide a roadmap for the subsequent identification of molecular target candidates of multiple cancer types.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenocarcinoma / diagnosis*
  • Adenocarcinoma / metabolism
  • Adenocarcinoma / pathology
  • Adult
  • Aged
  • Aged, 80 and over
  • Amino Acid Sequence
  • Annexin A4 / metabolism
  • Biomarkers, Tumor / chemistry
  • Biomarkers, Tumor / metabolism*
  • Blood Proteins / biosynthesis
  • Carcinoembryonic Antigen / blood
  • Claudin-3
  • Colorectal Neoplasms / diagnosis*
  • Colorectal Neoplasms / metabolism
  • Colorectal Neoplasms / pathology
  • Female
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Kaplan-Meier Estimate
  • Male
  • Membrane Proteins / biosynthesis
  • Membrane Proteins / blood
  • Membrane Proteins / chemistry
  • Membrane Proteins / metabolism*
  • Middle Aged
  • Molecular Diagnostic Techniques
  • Multivariate Analysis
  • Peptides / chemistry
  • Prognosis
  • Proportional Hazards Models
  • Proteome / chemistry
  • Proteome / metabolism*
  • ROC Curve
  • Tandem Mass Spectrometry / methods
  • alpha-Defensins / metabolism

Substances

  • Annexin A4
  • Biomarkers, Tumor
  • Blood Proteins
  • CLDN3 protein, human
  • Carcinoembryonic Antigen
  • Claudin-3
  • Membrane Proteins
  • Peptides
  • Proteome
  • STOML2 protein, human
  • alpha-Defensins
  • human neutrophil peptide 1