Exome sequencing and analysis of induced pluripotent stem cells identify the cilia-related gene male germ cell-associated kinase (MAK) as a cause of retinitis pigmentosa

Proc Natl Acad Sci U S A. 2011 Aug 23;108(34):E569-76. doi: 10.1073/pnas.1108918108. Epub 2011 Aug 8.

Abstract

Retinitis pigmentosa (RP) is a genetically heterogeneous heritable disease characterized by apoptotic death of photoreceptor cells. We used exome sequencing to identify a homozygous Alu insertion in exon 9 of male germ cell-associated kinase (MAK) as the cause of disease in an isolated individual with RP. Screening of 1,798 unrelated RP patients identified 20 additional probands homozygous for this insertion (1.2%). All 21 affected probands are of Jewish ancestry. MAK encodes a kinase involved in the regulation of photoreceptor-connecting cilium length. Immunohistochemistry of human donor tissue revealed that MAK is expressed in the inner segments, cell bodies, and axons of rod and cone photoreceptors. Several isoforms of MAK that result from alternative splicing were identified. Induced pluripotent stem cells were derived from the skin of the proband and a patient with non-MAK-associated RP (RP control). In the RP control individual, we found that a transcript lacking exon 9 was predominant in undifferentiated cells, whereas a transcript bearing exon 9 and a previously unrecognized exon 12 predominated in cells that were differentiated into retinal precursors. However, in the proband with the Alu insertion, the developmental switch to the MAK transcript bearing exons 9 and 12 did not occur. In addition to showing the use of induced pluripotent stem cells to efficiently evaluate the pathogenicity of specific mutations in relatively inaccessible tissues like retina, this study reveals algorithmic and molecular obstacles to the discovery of pathogenic insertions and suggests specific changes in strategy that can be implemented to more fully harness the power of sequencing technologies.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Alu Elements / genetics
  • Amino Acid Sequence
  • Biomarkers / metabolism
  • Cell Differentiation
  • Cilia / genetics*
  • Exons / genetics*
  • Genealogy and Heraldry
  • Humans
  • Induced Pluripotent Stem Cells / metabolism*
  • Isoenzymes / metabolism
  • Jews / genetics
  • Molecular Sequence Data
  • Mutagenesis, Insertional / genetics
  • Organ Specificity
  • Point Mutation / genetics
  • Protein Serine-Threonine Kinases / chemistry
  • Protein Serine-Threonine Kinases / genetics*
  • Retinal Cone Photoreceptor Cells / enzymology
  • Retinal Cone Photoreceptor Cells / pathology
  • Retinal Degeneration / complications
  • Retinal Degeneration / enzymology
  • Retinal Rod Photoreceptor Cells / enzymology
  • Retinal Rod Photoreceptor Cells / pathology
  • Retinitis Pigmentosa / complications
  • Retinitis Pigmentosa / enzymology*
  • Retinitis Pigmentosa / genetics*
  • Sequence Analysis, DNA*

Substances

  • Biomarkers
  • Isoenzymes
  • Protein Serine-Threonine Kinases
  • MAK protein, human