Aggregation of the protein TRIOBP-1 and its potential relevance to schizophrenia

PLoS One. 2014 Oct 21;9(10):e111196. doi: 10.1371/journal.pone.0111196. eCollection 2014.

Abstract

We have previously proposed that specific proteins may form insoluble aggregates as a response to an illness-specific proteostatic dysbalance in a subset of brains from individuals with mental illness, as is the case for other chronic brain conditions. So far, established risk factors DISC1 and dysbindin were seen to specifically aggregate in a subset of such patients, as was a novel schizophrenia-related protein, CRMP1, identified through a condition-specific epitope discovery approach. In this process, antibodies are raised against the pooled insoluble protein fractions (aggregomes) of post mortem brain samples from schizophrenia patients, followed by epitope identification and confirmation using additional techniques. Pursuing this epitope discovery paradigm further, we reveal TRIO binding protein (TRIOBP) to be a major substrate of a monoclonal antibody with a high specificity to brain aggregomes from patients with chronic mental illness. TRIOBP is a gene previously associated with deafness which encodes for several distinct protein species, each involved in actin cytoskeletal dynamics. The 3' splice variant TRIOBP-1 is found to be the antibody substrate and has a high aggregation propensity when over-expressed in neuroblastoma cells, while the major 5' splice variant, TRIOBP-4, does not. Endogenous TRIOBP-1 can also spontaneously aggregate, doing so to a greater extent in cell cultures which are post-mitotic, consistent with aggregated TRIOBP-1 being able to accumulate in the differentiated neurons of the brain. Finally, upon expression in Neuroscreen-1 cells, aggregated TRIOBP-1 affects cell morphology, indicating that TRIOBP-1 aggregates may directly affect cell development, as opposed to simply being a by-product of other processes involved in major mental illness. While further experiments in clinical samples are required to clarify their relevance to chronic mental illness in the general population, TRIOBP-1 aggregates are thus implicated for the first time as a biological element of the neuropathology of a subset of chronic mental illness.

Publication types

  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Actins / metabolism
  • Antibodies, Monoclonal / immunology
  • Autopsy
  • Brain / immunology
  • Brain / metabolism*
  • Brain / pathology
  • Cell Culture Techniques
  • Cell Differentiation / genetics
  • Epitopes / genetics
  • Epitopes / immunology
  • Humans
  • Microfilament Proteins / genetics
  • Microfilament Proteins / metabolism*
  • Neurites / metabolism
  • Neurites / pathology
  • Neurons / metabolism
  • Neurons / pathology
  • Protein Aggregates / genetics*
  • Protein Aggregates / immunology
  • Protein Aggregation, Pathological / genetics*
  • Protein Aggregation, Pathological / immunology
  • Protein Aggregation, Pathological / pathology
  • RNA Splice Sites / genetics
  • Schizophrenia / genetics*
  • Schizophrenia / metabolism
  • Schizophrenia / pathology
  • Synapsins / metabolism

Substances

  • Actins
  • Antibodies, Monoclonal
  • Epitopes
  • Microfilament Proteins
  • Protein Aggregates
  • RNA Splice Sites
  • Synapsins
  • TRIOBP protein, human

Grants and funding

This work was supported by the Alexander von Humboldt Foundation (www.humboldt-foundation.de), the Fritz Thyssen Foundation (www.fritz-thyssen-stiftung.de) and the Forschungskommission of the Medical Faculty of the Heinrich Heine University (www.medizin.hhu.de/dekanat/gremien-und-kommissionen/kommissionen/forschungskommission.html) to NJB. EU-FP6 (“cNEUPRO”, ec.europa.eu/research/fp6) to CK and SM, and the Stanley Medical Research Institute (02R-186, Baltimore, Maryland, United States of America, www.stanleyresearch.org), the Brain Behavior and Research Foundation (NARSAD Independent Investigator Award #20350, bbrfoundation.org/II), NEURON-ERANET (“DISCover”, BMBF 01EW1003, www.neuron-eranet.eu/en/196.php) and EU-FP7 (MC-ITN “IN-SENS” #607616, ec.europa.eu/research/mariecurieactions/about-mca/actions/itn/index_en.htm) to CK. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.