Effects of reduced mitochondrial DNA content on secondary mitochondrial toxicant exposure in Caenorhabditis elegans

Mitochondrion

Volumn 30, Issue , 2016, Pages 255-264

  Luz, Anthony L ^a   Meyer, Joel N ^a  

^a DUKE UNIVERSITY   (United States)

Author keywords

Arsenite; Caenorhabditis elegans; DNA damage; Environmental toxicant; mtDNA depletion; Ultraviolet C

Indexed keywords

ADENOSINE TRIPHOSPHATE; AFLATOXIN B1; ARSENIC TRIOXIDE; ETHIDIUM BROMIDE; MITOCHONDRIAL DNA; PARAQUAT; ROTENONE; DNA; INORGANIC COMPOUND; MUTAGENIC AGENT; ORGANIC COMPOUND;

ANIMAL EXPERIMENT; ARTICLE; CAENORHABDITIS ELEGANS; CONTROLLED STUDY; DNA CONTENT; DNA REPLICATION; ENVIRONMENTAL EXPOSURE; LIFESPAN; MITOCHONDRIAL RESPIRATION; NONHUMAN; PRIORITY JOURNAL; SENSITIZATION; STEADY STATE; ULTRAVIOLET C RADIATION; ANIMAL; DISEASE PREDISPOSITION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA DAMAGE; DRUG EFFECTS; METABOLISM; RADIATION RESPONSE; ULTRAVIOLET RADIATION;

ANIMALS; CAENORHABDITIS ELEGANS; DISEASE SUSCEPTIBILITY; DNA; DNA DAMAGE; DNA, MITOCHONDRIAL; ENVIRONMENTAL EXPOSURE; INORGANIC CHEMICALS; MITOCHONDRIAL DISEASES; MUTAGENS; ORGANIC CHEMICALS; ULTRAVIOLET RAYS;

EID: 84992187812     PISSN: 15677249     EISSN: 18728278     Source Type: Journal    
DOI: 10.1016/j.mito.2016.08.014     Document Type: Article

References (81)

1. [1] Anderson, S., et al. Sequence and Organization of the Human Mitochondrial Genome. 1981.
2. [2] Naviaux, R.K., Mitochondrial DNA disorders. Eur. J. Pediatr. 159:3 (2000), S219–S226.
3. [3] Wallace, D.C., A mitochondrial bioenergetic etiology of disease. J. Clin. Invest. 123:4 (2013), 1405–1412.
4. [4] García-Rodríguez, L.J., Appendix 1. Basic properties of mitochondria. Methods Cell Biol. 80 (2006), 809–812.
5. [5] Sarzi, E., et al. Mitochondrial DNA depletion is a prevalent cause of multiple respiratory chain deficiency in childhood. J. Pediatr. 150:5 (2007), 531–534, e6.
6. [6] Suomalainen, A., Isohanni, P., Mitochondrial DNA depletion syndromes–many genes, common mechanisms. Neuromuscul. Disord. 20:7 (2010), 429–437.
7. [7] El-Hattab, A.W., Scaglia, F., Mitochondrial DNA depletion syndromes: review and updates of genetic basis, manifestations, and therapeutic options. Neurotherapeutics 10:2 (2013), 186–198.
8. [8] Renaldo, F., et al. MFN2, a new gene responsible for mitochondrial DNA depletion. Brain, 135(8), 2012, e223.
9. [9] Rouzier, C., et al. The MFN2 gene is responsible for mitochondrial DNA instability and optic atrophy ‘plus’ phenotype. Brain, 2011, awr323.
10. [10] Poirier, M.C., et al. Long-term mitochondrial toxicity in HIV-uninfected infants born to HIV-infected mothers. J. Acquir. Immune Defic. Syndr. 33:2 (2003), 175–183.
11. [11] Divi, R.L., et al. Transplacentally exposed human and monkey newborn infants show similar evidence of nucleoside reverse transcriptase inhibitor-induced mitochondrial toxicity. Environ. Mol. Mutagen. 48:3–4 (2007), 201–209.
12. [12] Divi, R.L., et al. Progressive mitochondrial compromise in brains and livers of primates exposed in utero to nucleoside reverse transcriptase inhibitors (NRTIs). Toxicol. Sci., 2010, kfq235.
13. [13] Meyer, J.N., et al. Mitochondria as a target of environmental toxicants. Toxicol. Sci. 134:1 (2013), 1–17.
14. [14] Liu, P., Demple, B., DNA repair in mammalian mitochondria: much more than we thought?. Environ. Mol. Mutagen. 51:5 (2010), 417–426.
15. [15] González-Hunt, C.P., et al. Exposure to mitochondrial genotoxins and dopaminergic neurodegeneration in Caenorhabditis elegans. PLoS One, 9(12), 2014, e114459.
16. [16] Niranjan, B., Bhat, N., Avadhani, N., Preferential attack of mitochondrial DNA by aflatoxin B1 during hepatocarcinogenesis. Science 215:4528 (1982), 73–75.
17. [17] Niranjan, B.G., et al. Protection of mitochondrial genetic system against aflatoxin B1 binding in animals resistant to aflatoxicosis. Cancer Res. 46:7 (1986), 3637–3641.
18. [18] Backer, J.M., Weinstein, I.B., Interaction of benzo (a) pyrene and its dihydrodiol-epoxide derivative with nuclear and mitochondrial DNA in C3H10T½ cell cultures. Cancer Res. 42:7 (1982), 2764–2769.
19. [19] Tsang, W.Y., Lemire, B.D., The role of mitochondria in the life of the nematode, Caenorhabditis elegans. Biochim. Biophys. Acta (BBA) - Mol. Basis Dis. 1638:2 (2003), 91–105.
20. [20] Braeckman, B.P., Houthoofd, K., Vanfleteren, J.R., Intermediary metabolism. WormBook, T.C.e.R. Community WormBook, 2009.
21. [21] Okimoto, R., et al. The mitochondrial genomes of two nematodes, Caenorhabditis elegans and Ascaris suum. Genetics 130:3 (1992), 471–498.
22. [22] Lagido, C., McLaggan, D., Glover, L.A., A screenable in vivo assay for mitochondrial modulators using transgenic bioluminescent Caenorhabditis elegans. J. Vis. Exp., 104, 2015, e53083.
23. [23] Lagido, C., et al. Bridging the phenotypic gap: real-time assessment of mitochondrial function and metabolism of the nematode Caenorhabditis elegans. BMC Physiol., 8(1), 2008, 7.
24. [24] Beanan, M.J., Strome, S., Characterization of a germ-line proliferation mutation in C. elegans. Development 116:3 (1992), 755–766.
25. [25] Boyd, W.A., et al. Application of a mathematical model to describe the effects of chlorpyrifos on Caenorhabditis elegans development. PLoS One, 4(9), 2009, e7024.
26. [26] Lewis, J.A., Fleming, J.T., Basic culture methods. Methods Cell Biol. 48 (1995), 3–29.
27. [27] Stiernagle, T., Maintenance of C. elegans. C. elegans, 2, 1999, 51–67.
28. [28] Zheng, S.-Q., et al. Drug absorption efficiency in Caenorhbditis elegans delivered by different methods. PLoS One, 8(2), 2013, e56877.
29. [29] Croteau, D.L., et al. Cooperative damage recognition by UvrA and UvrB: identification of UvrA residues that mediate DNA binding. DNA Repair 7:3 (2008), 392–404.
30. [30] Rooney, J.P., et al. PCR based determination of mitochondrial DNA copy number in multiple species. Mitochondrial Regulation: Methods and Protocols, 2015, 23–38.
31. [31] Gonzalez-Hunt, C.P., et al. PCR-based analysis of mitochondrial DNA copy number, mitochondrial DNA damage, and nuclear DNA damage. Curr. Protoc. Toxicol., 2016, 20.11.1–20.11.25.
32. [32] Luz, A.L., et al. Seahorse Xfe24 extracellular flux analyzer-based analysis of cellular respiration in Caenorhabditis elegans. Curr. Protoc. Toxicol., 2015, 25.7. 1–25.7. 15.
33. [33] Luz, A.L., et al. Mitochondrial morphology and fundamental parameters of the mitochondrial respiratory chain are altered in Caenorhabditis elegans strains deficient in mitochondrial dynamics and homeostasis processes. PLoS One, 10(6), 2015, e0130940.
34. [34] Hoogewijs, D., et al. Selection and validation of a set of reliable reference genes for quantitative sod gene expression analysis in C. elegans. BMC Mol. Biol., 9(1), 2008, 1.
35. [35] Leung, M.C., et al. Effects of early life exposure to ultraviolet C radiation on mitochondrial DNA content, transcription, ATP production, and oxygen consumption in developing Caenorhabditis elegans. BMC Pharmacol. Toxicol., 14(1), 2013, 9.
36. [36] Luz, A.L., et al. Arsenite uncouples mitochondrial respiration and induces a Warburg-like effect in Caenorhabditis elegans. Toxicol. Sci., 2016.
37. [37] Luz, A., et al. In vivo determination of mitochondrial function using luciferase-expressing Caenorhabditis elegans: contribution of oxidative phosphorylation, glycolysis, and fatty acid oxidation to toxicant-induced dysfunction. Curr. Protoc. Toxicol. 69 (2016), 25.8.1–25.8.22.
38. [38] Tsang, W.Y., Lemire, B.D., Mitochondrial genome content is regulated during nematode development. Biochem. Biophys. Res. Commun. 291:1 (2002), 8–16.
39. [39] Gaines, G., Attardi, G., Intercalating drugs and low temperatures inhibit synthesis and processing of ribosomal RNA in isolated human mitochondria. J. Mol. Biol. 172:4 (1984), 451–466.
40. [40] Zylbee, E., Vesco, C., Penman, S., Selective inhibition of the synthesis of mitochondria-associated RNA by ethidium bromide. J. Mol. Biol. 44:1 (1969), 195–204.
41. [41] Nass, M.M., Differential effects of ethidium bromide on mitochondrial and nuclear DNA synthesis in vivo in cultured mammalian cells. Exp. Cell Res. 72:1 (1972), 211–222.
42. [42] Au, C., et al. SMF-1, SMF-2 and SMF-3 DMT1 orthologues regulate and are regulated differentially by manganese levels in C. elegans. PloS one, 4(11), 2009, e7792.
43. [43] Partridge, F.A., et al. The C. elegans glycosyltransferase BUS-8 has two distinct and essential roles in epidermal morphogenesis. Dev. Biol. 317:2 (2008), 549–559.
44. [44] Watanabe, M., et al. A mutation in a cuticle collagen causes hypersensitivity to the endocrine disrupting chemical, bisphenol A, in Caenorhabditis elegans. Mutat. Res. Fundam. Mol. Mech. Mutagen. 570:1 (2005), 71–80.
45. [45] Houtkooper, R.H., et al. Mitonuclear protein imbalance as a conserved longevity mechanism. Nature 497:7450 (2013), 451–457.
46. [46] Bess, A.S., et al. Mitochondrial dynamics and autophagy aid in removal of persistent mitochondrial DNA damage in Caenorhabditis elegans. Nucleic Acids Res., 2012, gks532.
47. [47] Poirier, M.C., et al. Fetal consequences of maternal antiretroviral nucleoside reverse transcriptase inhibitor use in human and nonhuman primate pregnancy. Curr. Opin. Pediatr. 27:2 (2015), 233–239.
48. [48] Shen, S., et al. Arsenic binding to proteins. Chem. Rev. 113:10 (2013), 7769–7792.
49. [49] Naranmandura, H., et al. Mitochondria are the main target organelle for trivalent monomethylarsonous acid (MMAIII)-induced cytotoxicity. Chem. Res. Toxicol. 24:7 (2011), 1094–1103.
50. [50] Zhao, F., et al. Arsenic exposure induces the Warburg effect in cultured human cells. Toxicol. Appl. Pharmacol. 271:1 (2013), 72–77.
51. [51] Tanner, C.M., et al. Rotenone, paraquat, and Parkinson's disease. Environ. Health Perspect. 119:6 (2011), 866–872.
52. [52] Kasiviswanathan, R., et al. Human mitochondrial DNA polymerase γ exhibits potential for bypass and mutagenesis at UV-induced cyclobutane thymine dimers. J. Biol. Chem. 287:12 (2012), 9222–9229.
53. [53] Meyer, J.N., et al. Decline of nucleotide excision repair capacity in aging Caenorhabditis elegans. Genome Biol., 8(5), 2007, R70.
54. [54] Fukami, J.-i., Yamamoto, I., Casida, J.E., Metabolism of rotenone in vitro by tissue homogenates from mammals and insects. Science 155:3763 (1967), 713–716.
55. [55] 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. 395:2 (2001), 158–168.
56. [56] Menzel, R., et al. CYP35: xenobiotically induced gene expression in the nematode Caenorhabditis elegans. Arch. Biochem. Biophys. 438:1 (2005), 93–102.
57. [57] Wolkow, C.A., Identifying factors that promote functional aging in Caenorhabditis elegans. Exp. Gerontol. 41:10 (2006), 1001–1006.
58. [58] Croll, N.A., Smith, J.M., Zuckerman, B.M., The aging process of the nematode Caenorhabditis elegans in bacterial and axenic culture. Exp. Aging Res. 3:3 (1977), 175–189.
59. [59] de Boer, R., et al. Caenorhabditis elegans as a model system for studying drug induced mitochondrial toxicity. PLoS One, 10(5), 2015.
60. [60] Bratic, I., et al. Mitochondrial DNA level, but not active replicase, is essential for Caenorhabditis elegans development. Nucleic Acids Res., 2009, gkp018.
61. [61] Divi, R.L., et al. Cardiac mitochondrial compromise in 1-yr-old Erythrocebus patas monkeys perinatally-exposed to nucleoside reverse transcriptase inhibitors. Cardiovasc. Toxicol. 5:3 (2005), 333–346.
62. [62] Altun, Z.F., Hall, D.H., Handbook of C. elegans anatomy. WormAtlas, 2005 http://www.wormatlas.org/ver1/handbook/contents.htm.
63. [63] Tsang, W.Y., et al. Mitochondrial respiratory chain deficiency in Caenorhabditis elegans results in developmental arrest and increased life span. J. Biol. Chem. 276:34 (2001), 32240–32246.
64. [64] Croy, R., et al. Identification of the principal aflatoxin B1-DNA adduct formed in vivo in rat liver. Proc. Natl. Acad. Sci. 75:4 (1978), 1745–1749.
65. [65] Quezada, T., et al. Effects of aflatoxin B1 on the liver and kidney of broiler chickens during development. Comp. Biochem. Physiol. C: Pharmacol. Toxicol. Endocrinol. 125:3 (2000), 265–272.
66. [66] Pan-Montojo, F., et al. Progression of Parkinson's disease pathology is reproduced by intragastric administration of rotenone in mice. PLoS One, 5(1), 2010, e8762.
67. [67] Ossowska, K., et al. Degeneration of dopaminergic mesocortical neurons and activation of compensatory processes induced by a long-term paraquat administration in rats: implications for Parkinson's disease. Neuroscience 141:4 (2006), 2155–2165.
68. [68] IARC, Some Drinking-water Disinfectants and Contaminants, Including Arsenic. IARC, 84, 2004.
69. [69] ATSDR, U., Toxicological Profile for Arsenic. 2007, Agency for Toxic Substances and Disease Registry, Division of Toxicology, Atlanta, GA.
70. [70] Juliani, M., Hixon, S., Moustacchi, E., Mitochondrial genetic damage induced in yeast by a photoactivated furocoumarin in combination with ethidium bromide or ultraviolet light. Mol. Gen. Genet. MGG 145:3 (1976), 249–254.
71. [71] Fuke, C., et al. [In vitro studies of the metabolism of paraquat and diquat using rat liver homogenates–isolation and identification of the metabolites of paraquat and diquat]. Nihon hoigaku zasshi. Jpn. J. Legal Med. 47:1 (1993), 33–45.
72. [72] Egner, P.A., et al. Identification of aflatoxin M1-N7-guanine in liver and urine of tree shrews and rats following administration of aflatoxin B1. Chem. Res. Toxicol. 16:9 (2003), 1174–1180.
73. [73] Mace, K., et al. Aflatoxin B1-induced DNA adduct formation and p53 mutations in CYP450-expressing human liver cell lines. Carcinogenesis 18:7 (1997), 1291–1297.
74. [74] Thomas, D.J., et al. Arsenic (+ 3 oxidation state) methyltransferase and the methylation of arsenicals. Exp. Biol. Med. 232:1 (2007), 3–13.
75. [75] Engström, K., et al. Polymorphisms in arsenic (+ III oxidation state) methyltransferase (AS3MT) predict gene expression of AS3MT as well as arsenic metabolism. Environ. Health Perspect., 119(2), 2011, 182.
76. [76] Calabrese, E.J., Baldwin, L.A., Inorganics and hormesis. Crit. Rev. Toxicol. 33:3–4 (2003), 215–304.
77. [77] Snow, E.T., et al. Arsenic, mode of action at biologically plausible low doses: what are the implications for low dose cancer risk?. Toxicol. Appl. Pharmacol. 207:2 (2005), 557–564.
78. [78] Baastrup, R., et al. Arsenic in drinking-water and risk for cancer in Denmark. Environ. Health Perspect., 116(2), 2008, 231.
79. [79] Schmeisser, S., et al. Mitochondrial hormesis links low-dose arsenite exposure to lifespan extension. Aging Cell 12:3 (2013), 508–517.
80. [80] Schmidt, C.M., et al. Hormesis effect of trace metals on cultured normal and immortal human mammary cells. Toxicol. Ind. Health 20:1–5 (2004), 57–68.
81. [81] Rooney, J., et al. Effects of 5′-fluoro-2-deoxyuridine on mitochondrial biology in Caenorhabditis elegans. Exp. Gerontol. 56 (2014), 69–76.