Epigenetics and DNA repair

Is a chromatin remodeling process involved in the higher UV sensitivity of nucleotide excision repair defective cells?

Marie Curie Project (FP7-IIF-221362/908362)

UVC irradiation induces two major DNA lesions: (I) cyclobutane pyrimidine dimers (CPDs) and (II) pyrimidine-pyrimidine 6-4 photoproducts (6-4 PP). Nucleotide excision repair (NER) is one of the major cellular pathways that remove the DNA lesions induced by UVC. Such lesions, if either unrepaired or misrepaired, interfere with essential DNA metabolic activities resulting in mutation induction, chromosomal instability and cell death (Friedberg et al., 1995).

The dramatic consequences of defective NER can be observed in the human hereditary diseases Xeroderma Pigmentosum (XP) and Cockayne's Syndrome (CS). XP and CS patients are extremely photosensitive and exhibit skeletal as well as neurological abnormalities. CS gene products are components of a special sub-pathway of NER known as transcription coupled repair (TCR). CS cells are then defective in the TCR pathway and are extremely sensitive to the cytotoxic effects of UVC irradiation (Boer and Hoeijmakers, 2000). It has been demonstrated that CS cells are prone to form chromosomal aberrations as well as to exhibit an enhanced apoptotic potential after UVC irradiation (De Santis et al., 2001).

AA8 and UV61 are isogenic Chinese hamster cell lines which differ in TCR efficiency. AA8 is the parental cell line, which is proficient in the genome overall repair of UVC radiation induced 6-4 PP and CPDs from the transcribing strand of active genes. UV61 cells (the hamster homologue of human Cockayne’s syndrome) originally isolated from AA8, exhibit proficient repair of 6-4 PP but are deficient in CPDs removal by the TCR pathway.

TCR is responsible for the accelerated removal of DNA lesions from the transcribing strand of active genes. Actively transcribing genes constitute 5-8% of the eukaryotic genome. The lesions repaired by TCR in those regions might be very minimal as compared to the remainder of the genome. Therefore, it can be expected only a slight increase in apoptosis and chromosomal aberrations in TCR defective UV61 cells as compared to AA8 cells. However, significant increase in the induction of both chromosomal aberrations and apoptosis were observed in UV61 cells (De Santis et al., 2001).

Since in Chinese hamster ovary cells lines (CHO) the global genome repair (GGR) is not active, the higher induction of chromosomal aberrations in CS cells seems to be associated with transcription blockage (TCR failure) caused by UV-lesions located in the transcribed strands of the genome. However, these lesions should not affect more than the 10% of the genome; therefore, it is proposed that the high increase in the production of chromosomal aberrations in CS cells could be related to a more decondensed chromatin in these cells after UVC exposure.

Preliminary experiments using the inhibitor of histone deacetylases trichostatin A (TSA), which produce a chromatin decondensation, showed a significant increase of chromosomal aberrations in normal as well as in CS cells treated with UVC in the presence of TSA. Since the formation of chromosomal aberrations derives from the repair process of primary UVC induced lesions, it has been proposed to study the influence of chromatin remodeling in the processing of UVC induced lesions in TCR proficient and deficient cell lines. Several methodological approaches were applied to study cell survival and proliferation with different doses of UVC and TSA to determine if any synergistic effect exists between both treatments. Then, kinetics analysis of UVC-induced CPDs repair in the presence or absence of TSA as well as the histone acetylation pattern along different recovery times after UVC irradiation were carried out. Finally, chromatin status was studied employing different approaches based in nucleases digestions on nuclei from treated and control cells to see whether there is any link between chromatin remodeling and the higher UVC sensitivity observed in CS cells.