Reprogramming to pluripotency can conceal somatic cell chromosomal instability

PLoS Genet. 2012;8(8):e1002913. doi: 10.1371/journal.pgen.1002913. Epub 2012 Aug 30.

Abstract

The discovery that somatic cells are reprogrammable to pluripotency by ectopic expression of a small subset of transcription factors has created great potential for the development of broadly applicable stem-cell-based therapies. One of the concerns regarding the safe use of induced pluripotent stem cells (iPSCs) in therapeutic applications is loss of genomic integrity, a hallmark of various human conditions and diseases, including cancer. Structural chromosome defects such as short telomeres and double-strand breaks are known to limit reprogramming of somatic cells into iPSCs, but whether defects that cause whole-chromosome instability (W-CIN) preclude reprogramming is unknown. Here we demonstrate, using aneuploidy-prone mouse embryonic fibroblasts (MEFs) in which chromosome missegregation is driven by BubR1 or RanBP2 insufficiency, that W-CIN is not a barrier to reprogramming. Unexpectedly, the two W-CIN defects had contrasting effects on iPSC genomic integrity, with BubR1 hypomorphic MEFs almost exclusively yielding aneuploid iPSC clones and RanBP2 hypomorphic MEFs karyotypically normal iPSC clones. Moreover, BubR1-insufficient iPSC clones were karyotypically unstable, whereas RanBP2-insufficient iPSC clones were rather stable. These findings suggest that aneuploid cells can be selected for or against during reprogramming depending on the W-CIN gene defect and present the novel concept that somatic cell W-CIN can be concealed in the pluripotent state. Thus, karyotypic analysis of somatic cells of origin in addition to iPSC lines is necessary for safe application of reprogramming technology.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Aneuploidy*
  • Animals
  • Cell Cycle Proteins
  • Cell Differentiation / genetics*
  • Cell Line
  • Chromosomal Instability / genetics*
  • Fibroblasts
  • Humans
  • Induced Pluripotent Stem Cells* / cytology
  • Induced Pluripotent Stem Cells* / metabolism
  • Mice
  • Molecular Chaperones / genetics
  • Molecular Chaperones / metabolism
  • Nuclear Pore Complex Proteins / genetics
  • Nuclear Pore Complex Proteins / metabolism
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism

Substances

  • Bub1b protein, mouse
  • Cell Cycle Proteins
  • Molecular Chaperones
  • Nuclear Pore Complex Proteins
  • ran-binding protein 2
  • BUB1 protein, human
  • Bub1 spindle checkpoint protein
  • Protein Serine-Threonine Kinases