Diagnosis of Constitutional Mismatch Repair-Deficiency Syndrome Based on Microsatellite Instability and Lymphocyte Tolerance to Methylating Agents

Gastroenterology. 2015 Oct;149(4):1017-29.e3. doi: 10.1053/j.gastro.2015.06.013. Epub 2015 Jun 25.

Abstract

Background & aims: Patients with bi-allelic germline mutations in mismatch repair (MMR) genes (MLH1, MSH2, MSH6, or PMS2) develop a rare but severe variant of Lynch syndrome called constitutional MMR deficiency (CMMRD). This syndrome is characterized by early-onset colorectal cancers, lymphomas or leukemias, and brain tumors. There is no satisfactory method for diagnosis of CMMRD because screens for mutations in MMR genes are noninformative for 30% of patients. MMR-deficient cancer cells are resistant to genotoxic agents and have microsatellite instability (MSI), due to accumulation of errors in repetitive DNA sequences. We investigated whether these features could be used to identify patients with CMMRD.

Methods: We examined MSI by PCR analysis and tolerance to methylating or thiopurine agents (functional characteristics of MMR-deficient tumor cells) in lymphoblastoid cells (LCs) from 3 patients with CMMRD and 5 individuals with MMR-proficient LCs (controls). Using these assays, we defined experimental parameters that allowed discrimination of a series of 14 patients with CMMRD from 52 controls (training set). We then used the same parameters to assess 23 patients with clinical but not genetic features of CMMRD.

Results: In the training set, we identified parameters, based on MSI and LC tolerance to methylation, that detected patients with CMMRD vs controls with 100% sensitivity and 100% specificity. Among 23 patients suspected of having CMMRD, 6 had MSI and LC tolerance to methylation (CMMRD highly probable), 15 had neither MSI nor LC tolerance to methylation (unlikely to have CMMRD), and 2 were considered doubtful for CMMRD based on having only 1 of the 2 features.

Conclusion: The presence of MSI and tolerance to methylation in LCs identified patients with CMMRD with 100% sensitivity and specificity. These features could be used in diagnosis of patients.

Keywords: Colon Cancer; Functional Tests; Predisposition; Tumor.

Publication types

  • Research Support, Non-U.S. Gov't
  • Validation Study

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adenosine Triphosphatases / genetics
  • Adult
  • Antineoplastic Agents, Alkylating / therapeutic use*
  • Biomarkers, Tumor / genetics*
  • Brain Neoplasms / diagnosis*
  • Brain Neoplasms / drug therapy
  • Brain Neoplasms / genetics
  • Brain Neoplasms / metabolism
  • Brain Neoplasms / pathology
  • Caco-2 Cells
  • Case-Control Studies
  • Colorectal Neoplasms / diagnosis*
  • Colorectal Neoplasms / drug therapy
  • Colorectal Neoplasms / genetics
  • Colorectal Neoplasms / metabolism
  • Colorectal Neoplasms / pathology
  • Colorectal Neoplasms, Hereditary Nonpolyposis / diagnosis*
  • Colorectal Neoplasms, Hereditary Nonpolyposis / drug therapy
  • Colorectal Neoplasms, Hereditary Nonpolyposis / genetics
  • Colorectal Neoplasms, Hereditary Nonpolyposis / metabolism
  • Colorectal Neoplasms, Hereditary Nonpolyposis / pathology
  • DNA Mutational Analysis
  • DNA Repair Enzymes / genetics
  • DNA-Binding Proteins / genetics
  • Drug Resistance, Neoplasm*
  • Female
  • Genetic Predisposition to Disease
  • Genetic Testing* / methods
  • Germ-Line Mutation*
  • HCT116 Cells
  • Heredity
  • Humans
  • Lymphocytes / drug effects*
  • Lymphocytes / metabolism
  • Male
  • Methylation
  • Microsatellite Instability*
  • Mismatch Repair Endonuclease PMS2
  • Multiplex Polymerase Chain Reaction
  • MutL Protein Homolog 1
  • MutS Homolog 2 Protein / genetics
  • Neoplastic Syndromes, Hereditary / diagnosis*
  • Neoplastic Syndromes, Hereditary / drug therapy
  • Neoplastic Syndromes, Hereditary / genetics
  • Neoplastic Syndromes, Hereditary / metabolism
  • Neoplastic Syndromes, Hereditary / pathology
  • Nuclear Proteins / genetics
  • Phenotype
  • Predictive Value of Tests
  • Reproducibility of Results
  • Transfection
  • Young Adult

Substances

  • Adaptor Proteins, Signal Transducing
  • Antineoplastic Agents, Alkylating
  • Biomarkers, Tumor
  • DNA-Binding Proteins
  • G-T mismatch-binding protein
  • MLH1 protein, human
  • Nuclear Proteins
  • Adenosine Triphosphatases
  • PMS2 protein, human
  • MSH2 protein, human
  • Mismatch Repair Endonuclease PMS2
  • MutL Protein Homolog 1
  • MutS Homolog 2 Protein
  • DNA Repair Enzymes

Supplementary concepts

  • Turcot syndrome