PUBLICATION

Cell stemness is maintained upon concurrent expression of RB and the mitochondrial ribosomal protein S18-2

Authors
Mushtaq, M., Kovalevska, L., Darekar, S., Abramsson, A., Zetterberg, H., Kashuba, V., Klein, G., Arsenian-Henriksson, M., Kashuba, E.
ID
ZDB-PUB-200624-6
Date
2020
Source
Proceedings of the National Academy of Sciences of the United States of America   117(27): 15673-15683 (Journal)
Registered Authors
Zetterberg, Henrik
Keywords
cell immortalization, embryogenesis, stemness and differentiation, tumorigenesis
MeSH Terms
  • Animals
  • Cell Differentiation/genetics
  • Cell Proliferation/genetics
  • Cell Self Renewal/genetics
  • Fibroblasts/metabolism
  • Gene Expression Regulation, Developmental/genetics
  • Histones/genetics
  • Human Embryonic Stem Cells/metabolism
  • Humans
  • Kruppel-Like Transcription Factors/genetics
  • Mice
  • Mitochondria/genetics*
  • Mitochondria/metabolism
  • Mouse Embryonic Stem Cells/metabolism*
  • Polycomb Repressive Complex 1/genetics
  • Retinoblastoma Binding Proteins/genetics*
  • Ribosomal Proteins/chemistry
  • Ribosomal Proteins/genetics*
  • Tumor Microenvironment/genetics
  • Ubiquitin-Protein Ligases/genetics
PubMed
32571933 Full text @ Proc. Natl. Acad. Sci. USA
Abstract
Stemness encompasses the capability of a cell for self-renewal and differentiation. The stem cell maintains a balance between proliferation, quiescence, and regeneration via interactions with the microenvironment. Previously, we showed that ectopic expression of the mitochondrial ribosomal protein S18-2 (MRPS18-2) led to immortalization of primary fibroblasts, accompanied by induction of an embryonic stem cell (ESC) phenotype. Moreover, we demonstrated interaction between S18-2 and the retinoblastoma-associated protein (RB) and hypothesized that the simultaneous expression of RB and S18-2 is essential for maintaining cell stemness. Here, we experimentally investigated the role of S18-2 in cell stemness and differentiation. Concurrent expression of RB and S18-2 resulted in immortalization of Rb1-/- primary mouse embryonic fibroblasts and in aggressive tumor growth in severe combined immunodeficiency mice. These cells, which express both RB and S18-2 at high levels, exhibited the potential to differentiate into various lineages in vitro, including osteogenic, chondrogenic, and adipogenic lineages. Mechanistically, S18-2 formed a multimeric protein complex with prohibitin and the ring finger protein 2 (RNF2). This molecular complex increased the monoubiquitination of histone H2ALys119, a characteristic trait of ESCs, by enhanced E3-ligase activity of RNF2. Furthermore, we found enrichment of KLF4 at the S18-2 promoter region and that the S18-2 expression is positively correlated with KLF4 levels. Importantly, knockdown of S18-2 in zebrafish larvae led to embryonic lethality. Collectively, our findings suggest an important role for S18-2 in cell stemness and differentiation and potentially also in cancerogenesis.
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