Oncotarget

Research Papers:

Involvement of MBD4 inactivation in mismatch repair-deficient tumorigenesis

Rossella Tricarico _, Salvatore Cortellino, Antonio Riccio, Shantie Jagmohan-Changur, Heleen van der Klift, Juul Wijnen, David Turner, Andrea Ventura, Valentina Rovella, Antonio Percesepe, Emanuela Lucci-Cordisco, Paolo Radice, Lucio Bertario, Monica Pedroni, Maurizio Ponz de Leon, Pietro Mancuso, Karthik Devarajan, Kathy Q. Cai, Andres J.P. Klein-Szanto, Giovanni Neri, Pål Møller, Alessandra Viel, Maurizio Genuardi, Riccardo Fodde and Alfonso Bellacosa

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Oncotarget. 2015; 6:42892-42904. https://doi.org/10.18632/oncotarget.5740

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Abstract

Rossella Tricarico1, Salvatore Cortellino2, Antonio Riccio3, Shantie Jagmohan-Changur4, Heleen Van der Klift5, Juul Wijnen5, David Turner6, Andrea Ventura7, Valentina Rovella8, Antonio Percesepe9, Emanuela Lucci-Cordisco10, Paolo Radice11, Lucio Bertario11, Monica Pedroni12, Maurizio Ponz de Leon12, Pietro Mancuso1,13, Karthik Devarajan14, Kathy Q. Cai15, Andres J.P. Klein-Szanto15, Giovanni Neri10, Pål Møller16, Alessandra Viel17, Maurizio Genuardi10, Riccardo Fodde4, Alfonso Bellacosa1

1Cancer Epigenetics and Cancer Biology Programs, Fox Chase Cancer Center, Philadelphia, Pennsylvania, United States

2IFOM-FIRC Institute of Molecular Oncology, Milan, Italy

3Department of Cardiology, Boston Children’s Hospital, Department of Neurobiology, Harvard Medical School, Boston, Massachusetts, United States

4Department of Pathology, Erasmus Medical Center Cancer Institute, Rotterdam, The Netherlands

5Department of Clinical Genetics and Department of Human Genetics, Leiden University Medical Center, Leiden, The Netherlands

6Department of Pathology and Laboratory Medicine, Medical University of South Carolina, Charleston, South Carolina, United States

7Cancer Biology and Genetics Program, Memorial Sloan Kettering Cancer Center, New York City, New York, United States

8Department of Systems Medicine, University of Rome Tor Vergata, Rome, Italy

9Medical Genetics Unit, Department of Mother & Child, University Hospital of Modena, Modena, Italy

10Institute of Medical Genetics, Catholic University of the Sacred Heart, “A. Gemelli” School of Medicine, Rome, Italy

11Department of Preventive and Predictive Medicine, Fondazione IRCCS Istituto Nazionale dei Tumori, Milano, Italy

12Department of Medicine and Public Health, University of Modena and Reggio Emilia, Modena, Italy

13Department of Medicine, Surgery and Neuroscience, University of Siena, Siena, Italy

14Department of Biostatistics, Fox Chase Cancer Center, Philadelphia, Pennsylvania, United States

15Department of Pathology, Fox Chase Cancer Center, Philadelphia, Pennsylvania, United States

16Inherited Cancer Research Group, Department for Medical Genetics, The Norwegian Radium Hospital, University Hospital, Oslo, Norway

17Experimental Oncology 1, CRO Aviano, National Cancer Institute, Aviano (PN), Italy

Correspondence to:

Alfonso Bellacosa, e-mail: [email protected]

Keywords: MBD4/MED1, HNPCC, colorectal cancer, mismatch repair, mutations

Received: June 10, 2015     Accepted: September 18, 2015     Published: October 16, 2015

ABSTRACT

The DNA glycosylase gene MBD4 safeguards genomic stability at CpG sites and is frequently mutated at coding poly-A tracks in mismatch repair (MMR)-defective colorectal tumors (CRC). Mbd4 biallelic inactivation in mice provided conflicting results as to its role in tumorigenesis. Thus, it is unclear whether MBD4 alterations are only secondary to MMR defects without functional consequences or can contribute to the mutator phenotype. We investigated MBD4 variants in a large series of hereditary/familial and sporadic CRC cases. Whereas MBD4 frameshifts were only detected in tumors, missense variants were found in both normal and tumor DNA. In CRC with double-MBD4/MMR and single-MBD4 variants, transition mutation frequency was increased, indicating that MBD4 defects may affect the mutational landscape independently of MMR defect. Mbd4-deficient mice showed reduced survival when combined with Mlh1−/− genotype. Taken together, these data suggest that MBD4 inactivation may contribute to tumorigenesis, acting as a modifier of MMR-deficient cancer phenotype.


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