Effects of early life exposure to ultraviolet C radiation on mitochondrial DNA content, transcription, ATP production, and oxygen consumption in developing Caenorhabditis elegans

BMC Pharmacology and Toxicology

Volumn 14, Issue , 2013, Pages

  Leung, Maxwell C K ^a   Rooney, John P ^a   Ryde, Ian T ^a   Bernal, Autumn J ^a   Bess, Amanda S ^a   Crocker, Tracey L ^a   Ji, Alex Q ^a   Meyer, Joel N ^a  

^a DUKE UNIVERSITY   (United States)

Author keywords

Caenorhabditis elegans; Early life exposure; Genotoxicity; Mitochondrial DNA damage; Mitochondrial dysfunction; Ultraviolet C radiation

Indexed keywords

ADENOSINE TRIPHOSPHATE; CELL NUCLEUS DNA; DNA DIRECTED DNA POLYMERASE GAMMA; MESSENGER RNA; MITOCHONDRIAL DNA; OXYGEN;

AEROBIC METABOLISM; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA CONTENT; DNA DAMAGE; DNA REPAIR; DNA TRANSCRIPTION; EARLY LIFE STRESS; ENZYME SYNTHESIS; GENE DOSAGE; GENE EXPRESSION; GENOTOXICITY; HEALTH HAZARD; LARVAL STAGE; MITOCHONDRIAL DYNAMICS; NONHUMAN; OXYGEN CONSUMPTION; RADIATION EXPOSURE; SOMATIC CELL; TRANSCRIPTOMICS; ULTRAVIOLET C RADIATION; UPREGULATION; ANIMAL; COPY NUMBER VARIATION; DNA MICROARRAY; GENE EXPRESSION PROFILING; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; ULTRAVIOLET RADIATION;

ADENOSINE TRIPHOSPHATE; ANIMALS; CAENORHABDITIS ELEGANS; DNA COPY NUMBER VARIATIONS; DNA DAMAGE; DNA, MITOCHONDRIAL; GENE EXPRESSION PROFILING; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OXYGEN CONSUMPTION; TRANSCRIPTION, GENETIC; ULTRAVIOLET RAYS;

MLCS; MLOWN;

EID: 84879826727     PISSN: 20506511     EISSN: None     Source Type: Journal    
DOI: 10.1186/2050-6511-14-9     Document Type: Article

References (64)

1. Schmidt CW. Mito-conundrum unraveling environmental effects on mitochondria. Environ Heal Perspect 2010, 118:A292-A297.
2. Shaughnessy DT, Worth L, Lawler CP, McAllister KA, Longley MJ, Copeland WC. Meeting report: Identification of biomarkers for early detection of mitochondrial dysfunction. Mitochondrion 2010, 10:579-581. 10.1016/j.mito.2010.02.001, 20197119.
3. Larsen NB, Rasmussen M, Rasmussen LJ. Nuclear and mitochondrial DNA repair: similar pathways?. Mitochondrion 2005, 5:89-108. 10.1016/j.mito.2005.02.002, 16050976.
4. Cohen BH. Pharmacologic effects on mitochondrial function. Dev Disabil Res Rev 2010, 16:189-199. 10.1002/ddrr.106, 20818734.
5. Gomez C, Bandez MJ, Navarro A. Pesticides and impairment of mitochondrial function in relation with the parkinsonian syndrome. Front Biosci 2007, 12:1079-1093. 10.2741/2128, 17127363.
6. Benhammou V, Tardieu M, Warszawski J, Rustin P, Blanche S. Clinical mitochondrial dysfunction in uninfected children born to HIV-infected mothers following perinatal exposure to nucleoside analogues. Environ Mol Mutagen 2007, 48:173-178. 10.1002/em.20279, 17358031.
7. Tsang WY, Lemire BD. The role of mitochondria in the life of the nematode, Caenorhabditis elegans. Biochim Biophys Acta 2003, 1638:91-105. 10.1016/S0925-4439(03)00079-6, 12853115.
8. Breton S, Stewart DT, Hoeh WR. Characterization of a mitochondrial ORF from the gender-associated mtDNAs of Mytilus spp. (Bivalvia: Mytilidae): Identification of the " missing" ATPase 8 gene. Mar Genom 2010, 3:11-18.
9. Tsang WY, Lemire BD. Mitochondrial genome content is regulated during nematode development. Biochem Biophys Res Commun 2002, 291:8-16. 10.1006/bbrc.2002.6394, 11829454.
10. Braeckman BP, Houthoofd K, Vanfleteren JR. Intermediary metabolism. WormBook 2009,
11. May-Panloup P, Chretien MF, Malthiery Y, Reynier P. Mitochondrial DNA in the oocyte and the developing embryo. Curr Top Dev Biol 2007, 77:51-83.
12. Shoubridge EA. Mitochondrial DNA segregation in the developing embryo. Hum Reprod 2000, 15(Suppl 2):229-234. 10.1093/humrep/15.suppl_2.229, 11041528.
13. Leung MC-K, Williams PL, Benedetto A, Au C, Helmke KJ, Aschner M, Meyer JN. Caenorhabditis elegans: an emerging model in biomedical and environmental toxicology. Toxicol Sci 2008, 106:5-28. 10.1093/toxsci/kfn121, 2563142, 18566021.
14. Furda AM, Marrangoni AM, Lokshin A, Van Houten B. Oxidants and not alkylating agents induce rapid mtDNA loss and mitochondrial dysfunction. DNA Repair (Amst) 2012, 11:684-692.
15. Bess AS, Crocker TL, Ryde IT, Meyer JN. Mitochondrial dynamics and autophagy aid in removal of persistent mitochondrial DNA damage in Caenorhabditis elegans. Nucleic Acids Res 2012, 40:7916-7931. 10.1093/nar/gks532, 3439916, 22718972.
16. Kasiviswanathan R, Gustafson MA, Copeland WC, Meyer JN. Human mitochondrial DNA polymerase gamma exhibits potential for bypass and mutagenesis at UV-induced cyclobutane thymine dimers. J Biol Chem 2012, 287:9222-9229. 10.1074/jbc.M111.306852, 3308766, 22194617.
17. Cline SD. Mitochondrial DNA damage and its consequences for mitochondrial gene expression. Biochim Biophys Acta 2012, 1819:979-991. 10.1016/j.bbagrm.2012.06.002, 22728831.
18. Lewis JA, Fleming JT. Basic Culture Methods. Caenorhabditis elegans: Modern Biological Analysis of an Organism 1995, 3-29. San Digo, CA: Academic Press, Epstein HF, Shakes DC.
19. Meyer JN, Boyd WA, Azzam GA, Haugen AC, Freedman JH, Van Houten B. Decline of nucleotide excision repair capacity in aging Caenorhabditis elegans. Genome Biol 2007, 8:R70. 10.1186/gb-2007-8-5-r70, 1929140, 17472752.
20. Lagido C, Pettitt J, Flett A, Glover LA. Bridging the phenotypic gap: real-time assessment of mitochondrial function and metabolism of the nematode Caenorhabditis elegans. BMC Physiol 2008, 8:7. 10.1186/1472-6793-8-7, 2364618, 18384668.
21. Simonis N, Rual JF, Carvunis AR, Tasan M, Lemmens I, Hirozane-Kishikawa T, Hao T, Sahalie JM, Venkatesan K, Gebreab F, et al. Empirically controlled mapping of the Caenorhabditis elegans protein-protein interactome network. Nat Methods 2009, 6:47-54. 10.1038/nmeth.1279, 3057923, 19123269.
22. Alfarano C, Andrade CE, Anthony K, Bahroos N, Bajec M, Bantoft K, Betel D, Bobechko B, Boutilier K, Burgess E, et al. The biomolecular interaction network database and related tools 2005 update. Nucleic Acids Res 2005, 33:D418-424. 540005, 15608229.
23. Zhong W, Sternberg PW. Genome-wide prediction of C. elegans genetic interactions. Science 2006, 311:1481-1484. 10.1126/science.1123287, 16527984.
24. Lee I, Lehner B, Crombie C, Wong W, Fraser AG, Marcotte EM. A single gene network accurately predicts phenotypic effects of gene perturbation in Caenorhabditis elegans. Nat Genet 2008, 40:181-188. 10.1038/ng.2007.70, 18223650.
25. Alexeyenko A, Sonnhammer EL. Global networks of functional coupling in eukaryotes from comprehensive data integration. Genome Res 2009, 19:1107-1116. 10.1101/gr.087528.108, 2694487, 19246318.
26. Ideker T, Ozier O, Schwikowski B, Siegel AF. Discovering regulatory and signalling circuits in molecular interaction networks. Bioinformatics 2002, 18(Suppl 1):S233-240. 10.1093/bioinformatics/18.suppl_1.S233, 12169552.
27. Maere S, Heymans K, Kuiper M. BiNGO: a Cytoscape plugin to assess overrepresentation of gene ontology categories in biological networks. Bioinformatics 2005, 21:3448-3449. 10.1093/bioinformatics/bti551, 15972284.
28. Bratic I, Hench J, Henriksson J, Antebi A, Burglin TR, Trifunovic A. Mitochondrial DNA level, but not active replicase, is essential for Caenorhabditis elegans development. Nucleic Acids Res 2009, 37:1817-1828. 10.1093/nar/gkp018, 2665216, 19181702.
29. Rozen S, Skaletsky H. Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 2000, 132:365-386.
30. Kodoyianni V, Maine EM, Kimble J. Molecular basis of loss-of-function mutations in the glp-1 gene of Caenorhabitis elegans. Mol Biol Cell 1992, 3:1199-1213. 275687, 1457827.
31. Sulston J. Cell Lineage. The Nematode Caenorhabditis elegans 1988, 123-155. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, Wood WB.
32. Golden TR, Beckman KB, Lee AH, Dudek N, Hubbard A, Samper E, Melov S. Dramatic age-related changes in nuclear and genome copy number in the nematode Caenorhabditis elegans. Aging Cell 2007, 6:179-188. 10.1111/j.1474-9726.2007.00273.x, 2049047, 17286610.
33. Emmons SW. The Genome. The Nematode Caenorhabditis elegans 1988, 47-79. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press, Wood WB.
34. Boyd WA, Crocker TL, Rodriguez AM, Leung MC, Lehmann DW, Freedman JH, Van Houten B, Meyer JN. Nucleotide excision repair genes are expressed at low levels and are not detectably inducible in Caenorhabditis elegans somatic tissues, but their function is required for normal adult life after UVC exposure. Mutat Res 2010, 683:57-67. 10.1016/j.mrfmmm.2009.10.008, 2799044, 19879883.
35. Hunter S, Jung D, Di Giulio R, Meyer J. The QPCR assay for analysis of mitochondrial DNA damage, repair, and relative copy number. Methods 2010, 51:444-451. 10.1016/j.ymeth.2010.01.033, 2912960, 20123023.
36. Hoogewijs D, Houthoofd K, Matthijssens F, Vandesompele J, Vanfleteren JR. Selection and validation of a set of reliable reference genes for quantitative sod gene expression analysis in C. elegans. BMC Mol Biol 2008, 9:9. 10.1186/1471-2199-9-9, 2254638, 18211699.
37. McLaggan D, Amezaga MR, Petra E, Frost A, Duff EI, Rhind SM, Fowler PA, Glover LA, Lagido C. Impact of sublethal levels of environmental pollutants found in sewage sluge on a novel Caenorhabditis elegans model biosensor. PLoS One 2012, 7(10):e46503. 10.1371/journal.pone.0046503, 3463613, 23056324.
38. Grad LI, Sayles LC, Lemire BD. Isolation and functional analysis of mitochondria from the nematode Caenorhabditis elegans. Methods Mol Biol 2007, 372:51-66. 10.1007/978-1-59745-365-3_4, 18314717.
39. Gaines G, Attardi G. Intercalating drugs and low temperatures inhibit synthesis and processing of ribosomal RNA in isolated human mitochondria. J Mol Biol 1984, 172:451-466. 10.1016/S0022-2836(84)80017-0, 6694216.
40. Hall DB, Kelley SO, Barton JK. Long-range and short-range oxidative damage to DNA: photoinduced damage to guanines in ethidium-DNA assemblies. Biochemistry 1998, 37:15933-15940. 10.1021/bi981750c, 9843399.
41. Kurbanyan K, Nguyen KL, To P, Rivas EV, Lueras AM, Kosinski C, Steryo M, Gonzalez A, Mah DA, Stemp ED. DNA-protein cross-linking via guanine oxidation: dependence upon protein and photosensitizer. Biochemistry 2003, 42:10269-10281. 10.1021/bi020713p, 12939156.
42. Ichishita R, Tanaka K, Sugiura Y, Sayano T, Mihara K, Oka T. An RNAi screen for mitochondrial proteins required to maintain the morphology of the organelle in Caenorhabditis elegans. J Biochem 2008, 143:449-454.
43. Lagido C, McLaggan D, Flett A, Pettitt J, Glover LA. Rapid sublethal toxicity assessment using bioluminescent Caenorhabditis elegans, a novel whole-animal metabolic biosensor. Toxicol Sci 2009, 109:88-95. 10.1093/toxsci/kfp058, 2721657, 19299418.
44. Houthoofd K, Braeckman BP, Lenaerts I, Brys K, De Vreese A, Van Eygen S, Vanfleteren JR. Ageing is reversed, and metabolism is reset to young levels in recovering dauer larvae of C. elegans. Exp Gerontol 2002, 37:1015-1021. 10.1016/S0531-5565(02)00063-3, 12213552.
45. Hunter SE, Gustafson MA, Margillo KM, Lee SA, Ryde IT, Meyer JN. In vivo repair of alkylating and oxidative DNA damage in the mitochondrial and nuclear genomes of wild-type and glycosylase-deficient Caenorhabditis elegans. DNA Repair (Amst) 2012, 11:857-863.
46. Baugh LR, Demodena J, Sternberg PW. RNA Pol II accumulates at promoters of growth genes during developmental arrest. Science 2009, 324:92-94. 10.1126/science.1169628, 19251593.
47. Menzel R, Bogaert T, Achazi R. A systematic gene expression screen of Caenorhabditis elegans cytochrome P450 genes reveals CYP35 as strongly xenobiotic inducible. Arch Biochem Biophys 2001, 395:158-168. 10.1006/abbi.2001.2568, 11697852.
48. Menzel R, Rodel M, Kulas J, Steinberg CE. CYP35: xenobiotically induced gene expression in the nematode Caenorhabditis elegans. Arch Biochem Biophys 2005, 438:93-102. 10.1016/j.abb.2005.03.020, 15910738.
49. Lindblom TH, Dodd AK. Xenobiotic detoxification in the nematode Caenorhabditis elegans. J Exp Zool 2006, 305:720-730.
50. Behan A, Doyle S, Farrell M. Adaptive responses to mitochondrial dysfunction in the rho degrees Namalwa cell. Mitochondrion 2005, 5:173-193. 10.1016/j.mito.2005.03.002, 16050983.
51. Tsang WY, Sayles LC, Grad LI, Pilgrim DB, Lemire BD. Mitochondrial respiratory chain deficiency in Caenorhabditis elegans results in developmental arrest and increased life span. J Biol Chem 2001, 276:32240-32246. 10.1074/jbc.M103999200, 11410594.
52. Ventura N, Rea SL, Schiavi A, Torgovnick A, Testi R, Johnson TE. p53/CEP-1 increases or decreases lifespan, depending on level of mitochondrial bioenergetic stress. Aging Cell 2009, 8:380-393. 10.1111/j.1474-9726.2009.00482.x, 2730656, 19416129.
53. Torgovnick A, Schiavi A, Testi R, Ventura N. A role for p53 in mitochondrial stress response control of longevity in C. elegans. Exp Gerontol 2010, 45:550-557. 10.1016/j.exger.2010.02.007, 20172019.
54. Mercer TR, Neph S, Dinger ME, Crawford J, Smith MA, Shearwood AM, Haugen E, Bracken CP, Rackham O, Stamatoyannopoulos JA, et al. The human mitochondrial transcriptome. Cell 2011, 146:645-658. 10.1016/j.cell.2011.06.051, 3160626, 21854988.
55. Durieux J, Wolff S, Dillin A. The cell-non-autonomous nature of electron transport chain-mediated longevity. Cell 2011, 144:79-91. 10.1016/j.cell.2010.12.016, 3062502, 21215371.
56. An JH, Blackwell TK. SKN-1 links C. elegans mesendodermal specification to a conserved oxidative stress response. Genes Dev 2003, 17:1882-1893. 10.1101/gad.1107803, 196237, 12869585.
57. Kahn NW, Rea SL, Moyle S, Kell A, Johnson TE. Proteasomal dysfunction activates the transcription factor SKN-1 and produces a selective oxidative-stress response in Caenorhabditis elegans. Biochem J 2008, 409:205-213. 10.1042/BJ20070521, 17714076.
58. Dingley S, Polyak E, Lightfoot R, Ostrovsky J, Rao M, Greco T, Ischiropoulos H, Falk MJ. Mitochondrial respiratory chain dysfunction variably increases oxidant stress in Caenorhabditis elegans. Mitochondrion 2010, 10:125-136. 10.1016/j.mito.2009.11.003, 19900588.
59. Bess AS, Ryde IT, Hinton DE, Meyer JN. UVC-induced mitochondrial degradation via autophagy correlates with mtDNA damage removal in primary human fibroblasts. J Biochem Mol Toxicol 27:28-41.
60. Piechota J, Szczesny R, Wolanin K, Chlebowski A, Bartnik E. Nuclear and mitochondrial genome responses in HeLa cells treated with inhibitors of mitochondrial DNA expression. Acta Biochim Pol 2006, 53:485-495.
61. Scarpulla RC. Nucleus-encoded regulators of mitochondrial function: Integration of respiratory chain expression, nutrient sensing and metabolic stress. Biochim Biophys Acta 2012, 1819:1088-1097. 10.1016/j.bbagrm.2011.10.011, 22080153.
62. Shutt TE, Lodeiro MF, Cotney J, Cameron CE, Shadel GS. Core human mitochondrial transcription apparatus is a regulated two-component system in vitro. Proc Natl Acad Sci USA 2010, 107:12133-12138. 10.1073/pnas.0910581107, 2901451, 20562347.
63. Chang DD, Clayton DA. Priming of human mitochondrial DNA replication occurs at the light-strand promoter. Proc Natl Acad Sci USA 1985, 82:351-355. 10.1073/pnas.82.2.351, 397036, 2982153.
64. Kasiviswanathan R, Collins TR, Copeland WC. The interface of transcription and DNA replication in the mitochondria. Biochim Biophys Acta 2012, 1819:970-978. 10.1016/j.bbagrm.2011.12.005, 22207204.