Degree Name

PhD (Doctor of Philosophy)

Program

Biomedical Sciences

Date of Award

12-2013

Committee Chair or Co-Chairs

Yue Zou, Ph.D.

Committee Members

Phillip R. Musich, Ph.D., William L. Stone, Ph.D., Krishna Singh, Ph.D., David A. Johnson, Ph.D.

Abstract

Integrity of the human genome is frequently threatened by endogenous and exogenous DNA damaging reagents that may lead to genome instability and cancer. Cells have evolved multiple mechanisms to repair DNA damage or to eliminate the damaged cells beyond repair and to prevent diverse diseases. Among these are ataxia telangiectasia and Rad3-related (ATR)-mediated DNA damage checkpoint and nucleotide excision repair (NER) that are the major pathways by which cells handle ultraviolet C (UV-C)- or other exogenous genotoxin-induced bulky DNA damage. However, it is unclear how these 2 pathways may be coordinated. In this study we show that ATR physically interacts with NER factor xeroderma pigmentosum group A (XPA) where an ATR phosphorylation site on serine 196 is located. Phosphorylation of XPA on serine 196 is required for repair of UV-induced DNA damage. In addition, a K188A point mutation of XPA that disrupts the ATR-XPA interaction inhibits the UV-induced XPA phosphorylation and DNA repair. Moreover, we show that depletion of p53, a downstream checkpoint of ATR, and inhibition of p53 transcriptional activities reduced the UV-induced XPA import. Furthermore, we found that the ATR-directed XPA nuclear import happens primarily in the S phase of the cell cycle. In effort to determine the mechanism involved in the XPA nuclear import, we found that, in addition to the nuclear localization signal (NLS) of XPA, importin-α4 is required for the UV-induced XPA nuclear import in an ATR-dependent manner. These data suggest that NER could be regulated by the ATR-dependent checkpoint via modulation of XPA phosphorylation and nuclear import. In a separate study we show that, upon UV damage, cytoplasmic ATR translocates to mitochondria, blocks the recruitment of proapoptotic Bcl-2–associated X (Bax) protein to mitochondria and prevents the loss of mitochondrial membrane potential (ΔΨ) and apoptosis. Bax-depletion reduces the effect of ATR on ΔΨ. Remarkably, the cytoplasmic ATR exhibits no checkpoint kinase activity, a hallmark function of nuclear ATR. Silencing of ATR’s kinase activity failed to affect Bax relocalization to mitochondria. These results reveal a novel checkpoint-independent antiapoptotic function of ATR at mitochondria in the cellular response to DNA damage.

Document Type

Dissertation - unrestricted

Copyright

Copyright by the authors.

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