Regulating transcriptional activity by phosphorylation: A new mechanism for the ARX homeodomain transcription factor

PLoS One. 2018 Nov 12;13(11):e0206914. doi: 10.1371/journal.pone.0206914. eCollection 2018.

Abstract

Aristaless-related homeobox (ARX) gene encodes a paired-type homeodomain transcription factor with critical roles in development. Here we identify that ARX protein is phosphorylated. Using mass spectrometry and in vitro kinase assays we identify phosphorylation at serines 37, 67 and 174. Through yeast-2-hybrid and CoIP we identified PICK1 (Protein interacting with C kinase 1) binding with the C-terminal region of ARX. PICK1 is a scaffold protein known to facilitate phosphorylation of protein partners by protein kinase C alpha (PRKCA). We confirm that ARX is phosphorylated by PRKCA and demonstrate phosphorylation at serine 174. We demonstrate that phosphorylation is required for correct transcriptional activity of the ARX protein using transcriptome-wide analysis of gene expression of phospho-null mutants (alanines replacing serines) compared to ARX wild-type (ARX-WT) overexpressed in pancreatic alpha TC cells. Compared to untransfected cells, ARX-WT overexpression significantly altered expression of 70 genes (Log2FC >+/-1.0, P-value <0.05). There were fewer genes with significantly altered expression compared to untransfected cells with the double phospho-null mutant Ser37Ala+Ser67Ala (26%) and Ser174Ala (39%), respectively. We demonstrate that the c-terminal region of ARX required to bind PICK1 causes a shift in PICK1 subcellular localisation to the nucleus to co-locate with the ARX protein, and truncation of this C-terminal region leads to the same loss of transcriptional activation as S174A mutant. In conclusion, we show that ARX is phosphorylated at several sites and that this modification affects its transcriptional activity.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Carrier Proteins / metabolism*
  • Cell Nucleus / metabolism
  • Gene Expression Profiling
  • Gene Expression Regulation, Developmental / physiology*
  • Glucagon-Secreting Cells
  • HEK293 Cells
  • Homeodomain Proteins / genetics
  • Homeodomain Proteins / metabolism*
  • Humans
  • Mice
  • Mutation
  • Nuclear Proteins / metabolism*
  • Phosphorylation / physiology*
  • Protein Kinase C-alpha / metabolism*
  • Serine / metabolism
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*

Substances

  • ARX protein, human
  • Carrier Proteins
  • Homeodomain Proteins
  • Nuclear Proteins
  • PICk1 protein, human
  • Transcription Factors
  • Serine
  • PRKCA protein, human
  • Protein Kinase C-alpha

Grants and funding

This research was supported by the Australian National Health and Medical Research Council (https://www.nhmrc.gov.au)- Project Grant 1063025 was awarded to CS; Australian Research Council Future Fellowship FT12100086 was awarded to CS; Channel 7 Children’s Research Foundation (https://crf.org.au) grant 14916, awarded to CS; and the MS McLeod Foundation (Women’s and Children’s Hospital, Adelaide awarded to support a PhD Scholarship to MHT (http://www.wch.sa.gov.au/research/funding/index_msmcleodpostgraduatescholarship.html). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.