Evolution of a Higher Intracellular Oxidizing Environment in Caenorhabditis elegans under Relaxed Selection

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Joyner Matos, Joanna ^a   Hicks, Kiley A ^b   Cousins, Dustin ^a   Keller, Michelle ^a   Denver, Dee R ^c   Baer, Charles F ^d   Estes, Suzanne ^b  

^a EASTERN WASHINGTON UNIVERSITY   (United States)

^b PORTLAND STATE UNIVERSITY   (United States)

^c OREGON STATE UNIVERSITY   (United States)

^d UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENINE; CYTOSINE; GUANINE; GUANOSINE; NUCLEOSIDE; RADICAL; THYMINE;

ARTICLE; BIOACCUMULATION; CAENORHABDITIS ELEGANS; CELL NUCLEUS; CONTROLLED STUDY; GENE MUTATION; GENETIC MARKER; GENETIC SELECTION; GENETIC TRAIT; GERM LINE; INSECT GENOME; MOLECULAR EVOLUTION; MUTATIONAL ANALYSIS; NONHUMAN; NUCLEIC ACID BASE SUBSTITUTION; OXIDATIVE STRESS; STEADY STATE; TISSUE SECTION;

ANIMALS; BIOLOGICAL EVOLUTION; CAENORHABDITIS ELEGANS; MUTATION; OXIDATIVE STRESS; SELECTION, GENETIC;

CAENORHABDITIS ELEGANS;

EID: 84878910873     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0065604     Document Type: Article

References (71)

1. Drake JW, Charlesworth B, Charlesworth D, Crow JF, (1998) Rates of spontaneous mutation. Genetics 148: 1667-1686.
2. Lynch M, Sung W, Morris K, Coffey N, Landry CR, et al. (2008) A genome-wide view of the spectrum of spontaneous mutations in yeast. Proc Nat Acad Sci USA 105: 9272-9277.
3. Hsie AW, Recio L, Katz DS, Lee CQ, Wagner M, et al. (1986) Evidence for reactive oxygen species inducing mutations in mammalian cells. Proc Nat Acad Sci USA 83: 9616-9620.
4. Gille JJP, van Berkel CGM, (1994) Mutagenicity of metabolic oxygen radicals in mammalian cell cultures. Carcinogenesis 15: 2695-2699.
5. Tudek B, (2003) Imidazole ring-opened DNA purines and their biological significance. J Biochem Molec Biol 36: 12-19.
6. Cooke MS, Evans MD, Dizdaroglu M, Lunec J, (2003) Oxidative DNA damage: mechanisms, mutation, and disease. FASEB J 17: 1195-1214.
7. Demple B, Harrison L, (1994) Repair of oxidative damage to DNA: Enzymology and biology. Annu Rev Biochem 63: 915-948.
8. Berquist BR, Wilson DMR, (2012) Pathways for repairing and tolerating the spectrum of oxidative DNA lesions. Cancer Lett 327: 61-72.
9. Tkeshelashvili LK, McBride T, Spence K, Loeb LA, (1991) Mutation spectrum of copper-induced DNA damage. J Biol Chem 266: 6401-6406.
10. Cheng KC, Cahill DS, Kasai H, Nishimura S, Loeb LA, (1992) 8-Hydroxyguanine, an abundant form of oxidative DNA damage, causes G>T and A>C substitutions. J Biol Chem 267: 166-172.
11. Maki H, Sekiguchi M, (1992) MutT protein specifically hydrolyses a potent mutagenic substrate for DNA synthesis. Nature 355: 273-275.
12. Cooke MS, Evans MD, (2007) 8-Oxo-deoxyguanosine: Reduce, reuse, recycle? Proc Nat Acad Sci USA 104: 13535-13536.
13. Busuttil RA, Garcia AM, Cabrera C, Rodriguez A, Suh Y, et al. (2005) Organ-specific increase in mutation accumulation and apoptosis rate in CuZn-superoxide dismutase-deficient mice. Cancer Res 65: 11271-11275.
14. Wallace DC, (2005) A mitochondrial paradigm of metabolic and degenerative diseases, aging, and cancer: A dawn for evolutionary medicine. Annu Rev Genet 39: 359-407.
15. Halliwell B, Gutteridge JMC (2007) Free Radicals in Biology and Medicine. London: Oxford University Press. 704 p.
16. Dollé MET, Snyder WK, Gossen JA, Lohman PHM, Vijg J, (2000) Distinct spectra of somatic mutations accumulated with age in mouse heart and small intestine. Proc Nat Acad Sci USA 97: 8403-8408.
17. Busuttil RA, Rubio M, Dollé MET, Campisi J, Vijg J, (2003) Oxygen accelerates the accumulation of mutations during the senescence and immortalization of murine cells in culture. Aging Cell 2: 287-294.
18. Paul C, Robaire B (2013) Ageing of the male germ line. Nat Rev Urol In press.
19. Denver DR, Dolan PC, Wilhelm LJ, Sung W, Lucas-Lledó JI, et al. (2009) A genome-wide view of Caenorhabditis elegans base substitution mutation process. Proc Nat Acad Sci USA 106: 16310-16324.
20. Kimura M, (1962) On the probability of fixation of mutant genes in a population. Genetics 47: 713-719.
21. Keightley PD, Caballero A, (1997) Genomic mutation rates for lifetime reproductive output and lifespan in Caenorhabditis elegans. Proc Nat Acad Sci USA 94: 3823-3827.
22. Kondrashov FA, Ogurtsov AY, Kondrashov AS, (2006) Selection in favor of nucleotides G and C diversifies evolution rates and levels of polymorphism at mammalian synonymous sites. J Theor Biol 240: 616-626.
23. Martin AP, Palumbi SR, (1993) Body size, metabolic rate, generation time, and the molecular clock. Proc Nat Acad Sci USA 90: 4087-4091.
24. Stoltzfus A, (2008) Evidence for a predominant role of oxidative damage in germline mutation in mammals. Mut Res 644: 71-73.
25. Agrawal AF, Wang AD, (2008) Increased transmission of mutations by low-condition females: Evidence for condition-dependent DNA repair. PLoS Biology 6: e30.
26. Sharp NP, Agrawal AF, (2012) Evidence for elevated mutation rates in low-quality genotypes. Proc Nat Acad Sci USA 109: 6142-6146.
27. Matsuba C, Lewis S, Ostrow DG, Salomon MP, Sylvestre L, et al. (2012) Invariance of mutational parameters for relative fitness over 400 generations of mutation accumulation in Caenorhabditis elegans. Genes, Genomes, Genetics 2: 1497-1503.
28. Baer CF, Shaw F, Steding C, Baumgartner M, Hawkins A, et al. (2005) Comparative evolutionary genetics of spontaneous mutations affecting fitness in rhabditid nematodes. Proc Nat Acad Sci USA 102: 5785-5790.
29. Denver DR, Wilhelm LJ, Howe DK, Gafner K, Dolan PC, et al. (2012) Variation in base-substitution mutation in experimental and natural lineages of Caenorhabditis nematodes. Genome Biol Evol 4: 513-522.
30. Denver DR, Feinberg S, Steding C, Durbin M, Lynch M, (2006) The relative roles of three DNA repair pathways in preventing Caenorhabditis elegans mutation accumulation. Genetics 174: 57-65.
31. Denver DR, Swenson SL, Lynch M, (2003) An evolutionary analysis of the helix-hairpin-helix superfamily of DNA repair glycosylases. Mol Biol Evol 20: 1603-1611.
32. Halligan DL, Keightley PD, (2009) Spontaneous mutation accumulation studies in evolutionary genetics. Annu Rev Ecol Evol Syst 40: 151-172.
33. Stiernagle T (1999) Maintenance of C. elegans. In: Hope IA, editor. C elegans: A Practical Approach. London: Oxford University Press. 51-67.
34. Estes S, Coleman-Hulbert A, Hicks KA, de Haan G, Martha SR, et al. (2011) Natural variation in life history and aging phenotypes is associated with mitochondrial DNA deletion frequency in Caenorhabditis elegans. BMC Evol Biol 11: 11.
35. Hicks KA, Howe DK, Leung A, Denver DR, Estes S, (2010) In vivo quantification reveals extensive natural variation in mitochondrial form and function in Caenorhabditis elegans. PLoS ONE 7: e43837.
36. Hicks KA, Denver DR, Estes S, (2013) Natural variation in Caenorhabditis briggsae mitochondrial form and function suggests a novel model of organelle dynamics. Mitochondrion 13: 44-51.
37. Zielonka J, Kalyanaraman B, (2010) Hydroethidine- and MitoSOX-derived red fluorescence is not a reliable indicator of intracellular superoxide formation, another inconvenient truth. Free Rad Biol Med 48: 983-1001.
38. Dingley S, Polyak E, Lightfoot R, Ostrovsky J, Rao M, et al. (2010) Mitochondrial respiratory chain dysfunction variably increases oxidant stress in Caenorhabditis elegans. Mitochondrion 10: 125-136.
39. Hartman P, Ponder R, Lo H-H, Ishii N, (2004) Mitochondrial oxidative stress can lead to nuclear hypermutability. Mech Ageing Dev 125: 417-420.
40. Cardoso AR, Chausse B, da Cunha FM, Luévano-Martínez LA, Marazzi TBM, et al. (2012) Mitochondrial compartmentalization of redox processes. Free Radic Biol Med 52: 2201-2208.
41. Delsite RL, Rasmussen LJ, Rasmussen AK, Kalen A, Goswami PC, et al. (2003) Mitochondrial impairment is accompanied by impaired oxidative DNA repair in the nucleus. Mutagenesis 18: 497-503.
42. Rowe LA, Degtyareva N, Doetsch PW, (2003) DNA damage-induced reactive oxygen species (ROS) stress response in Saccharomyces cerevisiae. Free Radic Biol Med 45: 1167-1177.
43. Dröge W, (2002) Free radicals in the physiological control of cell function. Physiol Rev 82: 47-95.
44. Adachi H, Fujiwara Y, Ishii N, (1998) Effects of oxygen on protein carbonyl and aging in Caenorhabditis elegans mutants with long (age-1) and short (mev-1) life spans. J Gerontol A Biol Sci Med Sci 53: B240-B244.
45. Yasuda K, Adachi H, Fujiwara Y, Ishii N, (1999) Protein carbonyl accumulation in aging dauer formation-defective (daf) mutants of Caenorhabditis elegans. J Gerontol A Biol Sci Med Sci 54: B47-51.
46. Arczewska KD, Baumeier C, Kassahun H, SenGupta T, Bjørås M, et al. (2011) Caenorhabditis elegans NDX-4 is a MutT-type enzyme that contributes to genomic stability. DNA Repair 10: 176-187.
47. Ishii N, Takahashi K, Tomita S, Keino T, Honda S, et al. (1990) A methyl viologen-sensitive mutant of the nematode Caenorhabditis elegans. Mutat Res 237: 165-171.
48. Ishii N, Fujii M, Hartman PS, Tsuda M, Yasuda K, et al. (1998) A mutation in succinate dehydrogenase cytochrome b causes oxidative stress and ageing in nematodes. Nature 394: 694-697.
49. Aitlhadj L, Stürzenbaum SR, (2010) The use of FUdR can cause prolonged longevity in mutant nematodes. Mech Ageing Dev 131: 364-365.
50. Gandhi S, Santelli J, Mitchell DH, Stiles JW, Sanadi DR, (1980) A simple method for maintaining large, aging populations of Caenorhabditis elegans. Mech Ageing Dev 12: 137-150.
51. Mitchell DH, Stiles JW, Santelli J, Sanadi DR, (1970) Synchronous growth and aging of Caenorhabditis elegans in the presence of fluorodeoxyuridine. J Gerontol 34: 28-36.
52. Ishii N, Senoo-Matsuda N, Miyake K, Yasuda K, Ishii T, et al. (2004) Coenzyme Q10 can prolong C. elegans lifespan by lowering oxidative stress. Mech Ageing Dev 125: 41-46.
53. Davies SK, Leroi AM, Bundy JG, (2012) Fluorodeoxyuridine affects the identification of metabolic responses to daf-2 status in Caenorhabditis elegans. Mech Ageing Dev 133: 46-49.
54. Yasuda K, Ishii T, Suda H, Akatsuka A, Hartman PS, et al. (2006) Age-related changes of mitochondrial structure and function in Caenorhabditis elegans. Mech Ageing Dev 127: 763-770.
55. Darr D, Fridovich I, (1995) Adaptation to oxidative stress in young, but not in mature or old, Caenorhabditis elegans. Free Rad Biol Med 18: 195-201.
56. Helbock HJ, Beckman KB, Shigenaga MK, Walter PB, Woodall AA, et al. (1998) DNA oxidation matters: The HPLC-electrochemical detection assay of 8-oxo-deoxyguanosine and 8-oxo-guanine. Proc Nat Acad Sci USA 95: 288-293.
57. Ishizawa M, Kobayashi Y, Miyamura T, Matsuura S (1991) Simple procedure of DNA isolation from human serum. Nucleic Acids Res 19: 5792.
58. Noguera JC, Kim S-Y, Velando A (2011) Pre-fledgling oxidative damage predicts recruitment in a long-lived bird. Biol Lett in press.
59. Kim S-Y, Velando A, Sorci G, Alonso-Alvarez C, (2010) Genetic correlation between resistance to oxidative stress and reproductive life span in a bird species. Evolution 64: 852-857.
60. Denver DR, Feinberg S, Estes S, Thomas WK, Lynch M, (2005) Mutation rates, spectra and hotspots in misatch repair-deficient Caenorhabditis elegans. Genetics 170: 107-113.
61. Baer CF, Denver DR, (2010) Spontaneous mutations decrease sensitivity of gene expression to random environmental variation in Caenorhabditis elegans. PLoS One 5: e8750.
62. Kondrashov AS, Houle D, (1994) Genotype-environment interactions and the estimation of the genomic mutation rate in Drosophila melanogaster. Proc R Soc Lond B 258: 221-227.
63. Garcia AM, Calder RB, Dollé MET, Lundell M, Kapahi P, et al. (2010) Age- and temperature-dependent somatic mutation accumulation in Drosophila melanogaster. PLoS Genetics 6: e10000950.
64. Busuttil RA, Garcia AM, Reddick RL, Dollé MET, Calder RB, et al. (2007) Intra-organ variation in age-related mutation accumulation in the mouse. PLoS ONE 2: e876.
65. Jeffreys AJ, Neumann R, (1997) Somatic mutation processes at a human minisatellite. Human Molec Genet 6: 129-136.
66. Fortune MT, Vassilopoulos C, Coolbaugh MI, Siciliano MJ, Monckton DG, (2000) Dramatic, expansion-biased, age-dependent, tissue-specific somatic mosaicism in a transgenic mouse model of triplet repeat instability. Human Molec Genet 9: 439-445.
67. Martorell L, Monckton DG, Gamez J, Baiget M, (2000) Complex patterns of male germline instability and somatic mosaicism in myotonic dystrophy type 1. Eur J Human Gen 8: 423-430.
68. Hill KA, Halangoda A, Heinmoeller PW, Gonzalez K, Chitaphan C, et al. (2005) Tissue-specific time courses of spontaneous mutation frequency and deviations in mutation pattern are observed in middle to late adulthood in Big Blue Mice. Environ Molec Mutag 45: 442-454.
69. Lynch M, (2010) Evolution of the mutation rate. Trends Genet 26: 345-352.
70. Uehara Y, Ikehata H, Furuya M, Kobayashi Y, He D, et al. (2009) XPC is involved in genome maintenance through multiple pathways in different tissues. Mut Res 670: 24-31.
71. Roerink SF, Koole W, Stapel LC, Romeijn RJ, Tijsterman M, (2012) A broad requirement for TLS polymerases η and κ, and interacting sumoylation and nuclear pore proteins, in lesion bypass during C. elegans embryogenesis. PLoS Genet 8: e1002800.