Homozygous mutation of MTPAP causes cellular radiosensitivity and persistent DNA double-strand breaks.
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2014 Mar 20;5:e1130. doi: 10.1038/cddis.2014.99.Homozygous mutation of MTPAP causes cellular radiosensitivity and persistent DNA double-strand breaks.1, 2, 3, 2, 2, 4, 4, 2, 5, 6, 2, 3, 7, 8.11] UCLA Department of Pathology and Laboratory Medicine, MacDonald Research Laboratories, Los Angeles, CA, USA [2] UCLA Biomedical Physics Interdepartmental Graduate Program, Los Angeles, CA, USA.2UCLA Department of Pathology and Laboratory Medicine, MacDonald Research Laboratories, Los Angeles, CA, USA.3Department of Public Health Sciences, Center for Public Health Genomics, University of Virginia, Charlottesville, VA, USA.4Genetics Institute, University of Florida, Gainesville, FL, USA.5UCLA Department of Pediatrics, Los Angeles, CA, USA.6Carle Physician Group, Urbana, IL, USA.71] UCLA Department of Pathology and Laboratory Medicine, MacDonald Research Laboratories, Los Angeles, CA, USA [2] UCLA Biomedical Physics Interdepartmental Graduate Program, Los Angeles, CA, USA [3] UCLA Department of Human Genetics, Los Angeles, CA, USA.81] Genetics Institute, University of Florida, Gainesville, FL, USA [2] Department of Pathology, Immunology and Laboratory Medicine, University of Florida, Gainesville, FL, USA.AbstractThe study of rare human syndromes characterized by radiosensitivity has been instrumental in identifying novel proteins and pathways involved in DNA damage responses to ionizing radiation. In the present study, a mutation in mitochondrial poly-A-polymerase (MTPAP), not previously recognized for its role in the DNA damage response, was identified by exome sequencing and subsequently associated with cellular radiosensitivity. Cell lines derived from two patients with the homozygous MTPAP missense mutation were radiosensitive, and this radiosensitivity could be abrogated by transfection of wild-type mtPAP cDNA into mtPAP-deficient cell lines. Further analysis of the cellular phenotype revealed delayed DNA repair, increased levels of DNA double-strand breaks, increased reactive oxygen species (ROS), and increased cell death after irradiation (IR). Pre-IR treatment of cells with the potent anti-oxidants, α-lipoic acid and n-acetylcysteine, was sufficient to abrogate the DNA repair and clonogenic survival defects. Our results firmly establish that mutation of the MTPAP gene results in a cellular phenotype of increased DNA damage, reduced repair kinetics, increased cell death by apoptosis, and reduced clonogenic survival after exposure to ionizing radiation, suggesting a pathogenesis that involves the disruption of ROS homeostasis. PMID:
[PubMed - indexed for MEDLINE] Cellular radiosensitivity and DNA repair defect segregated with affected members of RS63 family with a homozygous mutation of mtPAP. (a) The survival fraction (SF%) measured by the CSA (at 1 Gy) is reduced in the two members of the RS63 family, RS63-3 and -7, who are homozygous for the MTPAP mutation. The ‘#' indicates SF% representative of WT and highly radiosensitive (A-T) cells used for comparison in clinical radiosensitivity testing based on Sun et al. The ‘$' denotes patients for whom we were not able to generate an LCL. The ‘&' denotes that we were unable to obtain DNAs for MTPAP however, the father is an obligate heterozygote. (b) The neutral comet assay, measuring predominately DNA DSBs, reveals an AT-like DNA repair defect in RS63-3 and -7. Results are displayed as percent DNA repair (% repair) post-15 Gy and represent the return of comet tails to baseline levels at 5 h post-IR. An asterisk denotes statistical significance at P&0.05Cell Death Dis. ):e1130.Transfection of WT mtPAP into RS63-3 and -7 rescued radiosensitivity and DNA repair defects. (a) Transfection of WT mtPAP cDNA (+) into RS63-3 and -7 rescued the radiosensitive (i.e., reduced SF%) phenotype measured by the CSA (at 1 Gy). A (+) denotes transfection with WT mtPAP cDNA and (-) denotes transfection with an empty vector. (b) WT mtPAP (+) or control plasmid (-) was transfected into RS63-3 and -7; the WT mtPAP plasmid rescued the DNA DSB repair defect as measured by the NCA (at 15 Gy). ‘% DNA repair' represents the return to baseline tail moment (TM) measure of DNA damage 5 h post-IR and is the TMno IR/TM5h. An asterisk denotes statistical significance at P&0.05Cell Death Dis. ):e1130.Increased induction of DNA damage post-IR in RS63-3 and -7. (a) γ-H2AX irradiation-induced foci (IRIF) were increased at 1 h (post-2 Gy) in RS63-3 and -7 compared with WT levels. The results are expressed as the percentage of cells positive for four or more foci/nuclei (% Pos). WT4 is a representative WT response. Asterisks denote statistical significance at P&0.05. (b) DNA DSB levels were assessed immediately post-2 and -5 Gy. Increased levels of DSBs were observed in RS63-3 and -7. Asterisks indicate statistical significance at the P&0.05 level comparing RS63-3 and -7 (n=4, each) to both WT3 and WT4 (n=4, each)Cell Death Dis. ):e1130.RS63-3 and -7 LCLs had normal mitochondrial respiration but increased levels of ROS and apoptosis post-IR. (a) Mitochondrial respiration was measured by monitoring metabolism of the rezasurin dye and indicated WT-like, or normal, respiration in RS63-3 and -7. The results are displayed as relative fluorescent units (RFUs) of the metabolized rezasurin dye. WT3 is a representative WT-LCL response. AT5 is a representative A-T cell with a characteristic mitochondrial defect. (b) Mitochondrial bioenergetics were profiled using the XF24 Extracellular Flux Analyzer, and RS63-3 and -7 had increased maximal respiration levels after addition of FCCP, compared with WT-LCLs. WT5 is a representative WT-LCL response. The oxygen consumption ratio (OCR) was measured as an indicator of mitochondrial respiration. (c) Reactive oxygen species (ROS) levels were assessed using DCHF-DA dye (RFU). Increased IR-induced levels of ROS were noted in RS63-3 and -7. Asterisks denote statistical significance at the P&0.05 level comparing the +IR condition of the indicated sample to both of the WT4 and WT5 +IR conditions. (d) Apoptosis was determined by FACS analysis of cells positive for Annexin V staining 48 h post-10 Gy, and indicates increased post-IR apoptosis in RS63-3 and -7. Asterisks indicate statistical significance at the P&0.05 levelCell Death Dis. ):e1130.Anti-oxidant α-lipoic acid (α-LA) reduced initial γ-H2AX foci levels, rescued repair defect, and abrogated radiosensitivity in RS63-3 and -7. (a) γ-H2AX foci were assessed 1-h post-2 Gy after overnight treatment with α-LA or vehicle control (DMSO). Pre-IR treatment with α-LA &1 μM abrogated the increased γ-H2AX foci phenotype in RS63-3 and -7, restoring WT-like levels of γ-H2AX foci-positive cells. One asterisk indicates statistical significance at the P&0.05 level comparing α-LA-treated samples to vehicle control samples for each cell line. Two asterisks indicate significance at the P&0.05 level comparing vehicle control samples across cell lines. (b) Pre-IR treatment of RS63-3 and -7 with 1 μM α-LA abrogated the post-IR DNA repair defect measured by the NCA. Comets resulting from unrepaired DSBs were assessed post-15 Gy and results are presented as ‘% Repair', which is the return to baseline levels of damage 5-h post-IR (TMno IR/TM5h). Asterisks indicate statistical significance at the P&0.05 level when comparing α-LA-treated samples to vehicle control samples. (c) Cellular radiosensitivity, indicated by reduced SF% post-1 Gy, was rescued in RS63-3 and -7 by pre-treatment with 1 μM α-LA. Asterisks denote statistical significance at the P&0.05 level when comparing α-LA-treated samples to vehicle control samplesCell Death Dis. ):e1130.Publication TypesMeSH TermsSubstancesGrant SupportFull Text Sources
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paininthelowerback.mobi
paininthelowerback.museum
paininthelowerback.pro
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