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New paradigms in the repair of oxidative damage in human genome: mechanisms ensuring repair of mutagenic base lesions during replication and involvement of accessory proteins

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Abstract

Oxidized bases in the mammalian genome, which are invariably mutagenic due to their mispairing property, are continuously induced by endogenous reactive oxygen species and more abundantly after oxidative stress. Unlike bulky base adducts induced by UV and other environmental mutagens in the genome that block replicative DNA polymerases, oxidatively damaged bases such as 5-hydroxyuracil, produced by oxidative deamination of cytosine in the template strand, do not block replicative polymerases and thus need to be repaired prior to replication to prevent mutation. Following up our earlier studies, which showed that the Nei endonuclease VIII like 1 (NEIL1) DNA glycosylase, one of the five base excision repair (BER)-initiating enzymes in mammalian cells, has enhanced expression during the S-phase and higher affinity for replication fork-mimicking single-stranded (ss) DNA substrates, we recently provided direct experimental evidence for NEIL1’s role in replicating template strand repair. The key requirement for this event, which we named as the ‘cow-catcher’ mechanism of pre-replicative BER, is NEIL1’s non-productive binding (substrate binding without product formation) to the lesion base in ss DNA template to stall DNA synthesis, causing fork regression. Repair of the lesion in reannealed duplex is then carried out by NEIL1 in association with the DNA replication proteins. NEIL1 (and other BER-initiating enzymes) also interact with several accessory and non-canonical proteins including the heterogeneous nuclear ribonucleoprotein U and Y-box-binding protein 1 as well as high mobility group box 1 protein, whose precise roles in BER are still obscure. In this review, we have discussed the recent advances in our understanding of oxidative genome damage repair pathways with particular focus on the pre-replicative template strand repair and the role of scaffold factors like X-ray repairs cross-complementing protein 1 and poly (ADP-ribose) polymerase 1 and other accessory proteins guiding distinct BER sub-pathways.

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Acknowledgments

The authors’ research is supported by US Public Health Services Research grants R01 CA158910 (SM), R01 GM105090 (SM), P01 CA92584 (SM), and Muscular Dystrophy Association (MDA 294842; MLH) and ALS Association (ALSA 15-IIP-204; MLH).

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Authors and Affiliations

  1. Department of Radiation Oncology, Houston Methodist Research Institute, Houston, TX, 77030, USA

    Arijit Dutta, Chunying Yang, Shiladitya Sengupta, Sankar Mitra & Muralidhar L. Hegde

  2. Department of Biochemistry and Molecular Biology, University of Texas Medical Branch, Galveston, TX, 77555, USA

    Arijit Dutta & Sankar Mitra

  3. Houston Methodist Neurological Institute, Houston, TX, 77030, USA

    Muralidhar L. Hegde

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  1. Arijit Dutta
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  2. Chunying Yang
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  3. Shiladitya Sengupta
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  4. Sankar Mitra
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  5. Muralidhar L. Hegde
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Correspondence to Sankar Mitra or Muralidhar L. Hegde.

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Dutta, A., Yang, C., Sengupta, S. et al. New paradigms in the repair of oxidative damage in human genome: mechanisms ensuring repair of mutagenic base lesions during replication and involvement of accessory proteins. Cell. Mol. Life Sci. 72, 1679–1698 (2015). https://doi.org/10.1007/s00018-014-1820-z

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  • DOI: https://doi.org/10.1007/s00018-014-1820-z

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