Caenorhabditis elegans as a model system for studying drug induced mitochondrial toxicity

PLoS ONE

Volumn 10, Issue 5, 2015, Pages

  De Boer, Richard ^a   Smith, Ruben L ^a   DeVos, Winnok H ^b,c   Manders, Erik M M ^a   Brul, Stanley ^a   Van Der Spek, Hans ^a  

^a UNIVERSITY OF AMSTERDAM   (Netherlands)

^b UNIVERSITY OF ANTWERP   (Belgium)

^c GHENT UNIVERSITY   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

DNA DIRECTED DNA POLYMERASE GAMMA; MITOCHONDRIAL DNA; 2',3' DIDEOXYNUCLEOSIDE DERIVATIVE; 3' FLUOROTHYMIDINE; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; DIDANOSINE; DNA DIRECTED DNA POLYMERASE; MITOCHONDRIAL PROTEIN; RNA DIRECTED DNA POLYMERASE INHIBITOR; STAVUDINE; UBIQUINONE; UBIQUINONE 9; ZALCITABINE; ZIDOVUDINE;

ADULT; ARTICLE; BINDING AFFINITY; CAENORHABDITIS ELEGANS; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DNA METABOLISM; ENTROPY; ENZYME ACTIVITY; EUKARYOTE; FLUORESCENCE MICROSCOPY; MITOCHONDRIAL TOXICITY; MITOCHONDRION; MORPHOLOGY; NONHUMAN; OXIDATION REDUCTION STATE; OXYGEN CONSUMPTION; PROTEIN BINDING; PROTEIN DEPLETION; QUANTITATIVE ANALYSIS; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; YOUNG ADULT; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; DRUG EFFECTS; DRUG SCREENING; GENETICS; HUMAN; METABOLISM; PROCEDURES; ULTRASTRUCTURE;

CAENORHABDITIS; CAENORHABDITIS ELEGANS; HUMAN IMMUNODEFICIENCY VIRUS 1;

ANIMALS; ANTI-HIV AGENTS; CAENORHABDITIS ELEGANS; DIDANOSINE; DIDEOXYNUCLEOSIDES; DNA, MITOCHONDRIAL; DNA-DIRECTED DNA POLYMERASE; DRUG EVALUATION; HUMANS; MITOCHONDRIA; MITOCHONDRIAL PROTEINS; MODELS, BIOLOGICAL; OXYGEN CONSUMPTION; REVERSE TRANSCRIPTASE INHIBITORS; STAVUDINE; UBIQUINONE; ZALCITABINE; ZIDOVUDINE;

EID: 84929376788     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0126220     Document Type: Article

References (50)

1. Zeviani M, Carelli V. Mitochondrial disorders. Curr Opin Neurol. 2007/09/22 ed. 2007; 20: 564-71. doi: 10.1097/WCO.0b013e3282ef58cd PMID: 17885446
2. Neustadt J, Pieczenik SR. Medication-induced mitochondrial damage and disease. Mol Nutr Food Res. 2008; 52: 780-8. doi: 10.1002/mnfr.200700075 PMID: 18626887
3. Brinkman K, ter Hofstede HJ, Burger DM, Smeitink JA, Koopmans PP. Adverse effects of reverse transcriptase inhibitors: mitochondrial toxicity as common pathway. Aids. 1998; 12: 1735-1744. PMID: 9792373
4. Brinkman K, Smeitink JA, Romijn JA, Reiss P. Mitochondrial toxicity induced by nucleoside-analogue reverse-transcriptase inhibitors is a key factor in the pathogenesis of antiretroviral-therapy-related lipodystrophy. Lancet. 1999; 354: 1112-5. doi: 10.1016/S0140-6736(99)06102-4 PMID: 10509516
5. Johnson AA, Ray AS, Hanes J, Suo Z, Colacino JM, Anderson KS, et al. Toxicity of antiviral nucleoside analogs and the human mitochondrial DNA polymerase. J Biol Chem. 2001; 276: 40847-57. doi: 10. 1074/jbc.M106743200 PMID: 11526116
6. Carr A, Cooper DA. Adverse effects of antiretroviral therapy. Lancet. 2000; 356: 1423-1430. PMID: 11052597
7. May MT, Ingle SM. Life expectancy of HIV-positive adults: a review. Sex Health. 2011; 8: 526-33. doi: 10.1071/SH11046 PMID: 22127039
8. Hammer SM, Eron JJ Jr, Reiss P, Schooley RT, Thompson MA, Walmsley S, et al. Antiretroviral treatment of adult HIV infection: 2008 recommendations of the International AIDS Society-USA panel. JAMA. 2008/08/05 ed. 2008; 300: 555-570. 300/5/555 [pii] doi: 10.1001/jama.300.5.555 PMID: 18677028
9. Apostolova N, Blas-García A, Esplugues J V. Mitochondrial interference by anti-HIV drugs: mechanisms beyond Pol-γ inhibition. Trends Pharmacol Sci. 2011/09/09 ed. 2011; 32: 715-25. doi: 10.1016/j. tips.2011.07.007 PMID: 21899897
10. Davidson I, Beardsell H, Smith B, Mandalia S, Bower M, Gazzard B, et al. The frequency and reasons for antiretroviral switching with specific antiretroviral associations: the SWITCH study. Antiviral Res. 2010; 86: 227-9. doi: 10.1016/j.antiviral.2010.03.001 PMID: 20211651
11. Schapira AH V. Mitochondrial diseases. Lancet. 2012; 379: 1825-34. doi: 10.1016/S0140-6736(11) 61305-6 PMID: 22482939
12. Lewis W, Dalakas MC. Mitochondrial toxicity of antiviral drugs. Nat Med. 1995/05/01 ed. 1995; 1: 417-22. PMID: 7585087
13. Lewis W, Kohler JJ, Hosseini SH, Haase CP, Copeland WC, Bienstock RJ, et al. Antiretroviral nucleosides, deoxynucleotide carrier and mitochondrial DNA: evidence supporting the DNA pol gamma hypothesis. AIDS. 2006; 20: 675-84. doi: 10.1097/01.aids.0000216367.23325.58 PMID: 16514297
14. Maagaard A, Kvale D. Long term adverse effects related to nucleoside reverse transcriptase inhibitors: clinical impact of mitochondrial toxicity. Scand J Infect Dis. 2009/11/20 ed. 2009; 41: 808-17. doi: 10. 3109/00365540903186181 PMID: 19922062
15. Kakuda TN. Pharmacology of nucleoside and nucleotide reverse transcriptase inhibitor-induced mitochondrial toxicity. Clin Ther. 2000/08/10 ed. 2000; 22: 685-708. doi: 10.1016/S0149-2918(00)90004-3 PMID: 10929917
16. Smith RL, de Boer R, Brul S, Budovskaya Y, van Spek H. Premature and accelerated aging: HIV or HAART? Front Genet. 2012; 3: 328. doi: 10.3389/fgene.2012.00328 PMID: 23372574
17. Markaki M, Tavernarakis N. Modeling human diseases in Caenorhabditis elegans. Biotechnol J. 2010; 5: 1261-76. doi: 10.1002/biot.201000183 PMID: 21154667
18. Culetto E, Sattelle DB. A role for Caenorhabditis elegans in understanding the function and interactions of human disease genes. Hum Mol Genet. 2000; 9: 869-877. PMID: 10767309
19. Chen X, Thorburn DR, Wong L-J, Vladutiu GD, Haas RH, Le T, et al. Quality improvement of mitochondrial respiratory chain complex enzyme assays using Caenorhabditis elegans. Genet Med. 2011; 13: 794-9. doi: 10.1097/GIM.0b013e31821afca5 PMID: 21633293
20. Addo MG, Cossard R, Pichard D, Obiri-Danso K, Rötig A, Delahodde A. Caenorhabditis elegans, a pluricellular model organism to screen new genes involved in mitochondrial genome maintenance. Biochim Biophys Acta. Elsevier B.V.; 2010; 1802: 765-73. doi: 10.1016/j.bbadis.2010.05.007 PMID: 20580819
21. Bratic I, Trifunovic A. Mitochondrial energy metabolism and ageing. Biochim Biophys Acta. Elsevier B. V.; 2010; 1797: 961-7. doi: 10.1016/j.bbabio.2010.01.004 PMID: 20064485
22. Tsang WY, Lemire BD. The role of mitochondria in the life of the nematode, Caenorhabditis elegans. Biochim Biophys Acta. 2003; 1638: 91-105. PMID: 12853115
23. Zubovych IO, Straud S, Roth MG. Mitochondrial dysfunction confers resistance to multiple drugs in Caenorhabditis elegans. Mol Biol Cell. 2010; 21: 956-69. doi: 10.1091/mbc.E09-08-0673 PMID: 20089839
24. Li J, Cai T, Wu P, Cui Z, Chen X, Hou J, et al. Proteomic analysis of mitochondria from Caenorhabditis elegans. Proteomics. 2009; 9: 4539-53. doi: 10.1002/pmic.200900101 PMID: 19670372
25. Smith RL, De Vos WH, de Boer R, Manders EMM, van der Spek H. In vivo visualization and quantification of mitochondrial morphology in C. elegans. Methods Mol Biol. 2015; 1265: 367-77. doi: 10.1007/ 978-1-4939-2288-8-26 PMID: 25634288
26. Artal-Sanz M, Tsang WY, Willems EM, Grivell LA, Lemire BD, van der Spek H, et al. The mitochondrial prohibitin complex is essential for embryonic viability and germline function in Caenorhabditis elegans. J Biol Chem. 2003; 278: 32091-9. doi: 10.1074/jbc.M304877200 PMID: 12794069
27. Grad LI, Sayles LC, Lemire BD. Introduction of an additional pathway for lactate oxidation in the treatment of lactic acidosis and mitochondrial dysfunction in Caenorhabditis elegans. Proc Natl Acad Sci U S A. 2005; 102: 18367-72. doi: 10.1073/pnas.0506939102 PMID: 16344465
28. Tsang WY, Lemire BD. Mitochondrial genome content is regulated during nematode development. Biochem Biophys Res Commun. 2002; 291: 8-16. doi: 10.1006/bbrc.2002.6394 PMID: 11829454
29. Côté HCF, Brumme ZL, Craib KJP, Alexander CS, Wynhoven B, Ting L, et al. Changes in mitochondrial DNA as a marker of nucleoside toxicity in HIV-infected patients. N Engl J Med. 2002; 346: 811-20. doi: 10.1056/NEJMoa012035 PMID: 11893792
30. O'Rourke EJ, Soukas AA, Carr CE, Ruvkun G. C. elegans major fats are stored in vesicles distinct from lysosome-related organelles. Cell Metab. 2009; 10: 430-5. doi: 10.1016/j.cmet.2009.10.002 PMID: 19883620
31. Mitchell DH, Stiles JW, Santelli J, Sanadi DR. Synchronous growth and aging of Caenorhabditis elegans in the presence of fluorodeoxyuridine. J Gerontol. 1979; 34: 28-36. PMID: 153363
32. Cihlar T, Ray AS. Nucleoside and nucleotide HIV reverse transcriptase inhibitors: 25 years after zidovudine. Antiviral Res. 2010; 85: 39-58. doi: 10.1016/j.antiviral.2009.09.014 PMID: 19887088
33. Bratic I, Hench J, Henriksson J, Antebi A, Bürglin TR, Trifunovic A. Mitochondrial DNA level, but not active replicase, is essential for Caenorhabditis elegans development. Nucleic Acids Res. 2009/02/03 ed. 2009; 37: 1817-28. doi: 10.1093/nar/gkp018 PMID: 19181702
34. Dykens JA, Will Y, editors. Drug-Induced Mitochondrial Dysfunction. Hoboken, NJ, USA: John Wiley &Sons, Inc.; 2008. doi: 10.1002/9780470372531
35. Martin JL, Brown CE, Matthews-Davis N, Reardon JE. Effects of antiviral nucleoside analogs on human DNA polymerases and mitochondrial DNA synthesis. Antimicrob Agents Chemother. 1994; 38: 2743-9. PMID: 7695256
36. Doléans-Jordheim A, Bergeron E, Bereyziat F, Ben-Larbi S, Dumitrescu O, Mazoyer M-A, et al. Zidovudine (AZT) has a bactericidal effect on enterobacteria and induces genetic modifications in resistant strains. Eur J Clin Microbiol Infect Dis. 2011; 30: 1249-56. doi: 10.1007/s10096-011-1220-3 PMID: 21494911
37. Vasta V, Sedensky M, Morgan P, Hahn SH. Altered redox status of coenzyme Q9 reflects mitochondrial electron transport chain deficiencies in Caenorhabditis elegans. Mitochondrion. 2011; 11: 136-138. doi: 10.1016/j.mito.2010.09.002 PMID: 20849980
38. Chen H, Vermulst M, Wang YE, Chomyn A, Prolla TA, McCaffery JM, et al. Mitochondrial fusion is required for mtDNA stability in skeletal muscle and tolerance of mtDNA mutations. Cell. 2010/04/21 ed. 2010; 141: 280-9. doi: 10.1016/j.cell.2010.02.026 PMID: 20403324
39. Pezeshkpour G, Illa I, Dalakas MC. Ultrastructural characteristics and DNA immunocytochemistry in human immunodeficiency virus and zidovudine-associated myopathies. Hum Pathol. 1991; 22: 1281-8. PMID: 1748434
40. Labrousse AM, Zappaterra MD, Rube DA, van der Bliek AM. C. elegans dynamin-related protein DRP-1 controls severing of the mitochondrial outer membrane. Mol Cell. 1999; 4: 815-26. PMID: 10619028
41. Lund KC, Wallace KB. Adenosine 3′,5′-cyclic monophosphate (cAMP)-dependent phosphoregulation of mitochondrial complex I is inhibited by nucleoside reverse transcriptase inhibitors. Toxicol Appl Pharmacol. 2008; 226: 94-106. doi: 10.1016/j.taap.2007.08.015 PMID: 17904600
42. 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: 7916-31. doi: 10.1093/nar/gks532 PMID: 22718972
43. Suntres ZE. Role of antioxidants in paraquat toxicity. Toxicology. 2002; 180: 65-77. PMID: 12324200
44. Koczor CA, Lewis W. Nucleoside reverse transcriptase inhibitor toxicity and mitochondrial DNA. Expert Opin Drug Metab Toxicol. 2010; 6: 1493-504. doi: 10.1517/17425255.2010.526602 PMID: 20929279
45. Skovgaard T, Uhlin U, Munch-Petersen B. Comparative active-site mutation study of human and Caenorhabditis elegans thymidine kinase 1. FEBS J. 2012; 279: 1777-87. doi: 10.1111/j.1742-4658.2012. 08554.x PMID: 22385435
46. Zeldin RK, Petruschke RA. Pharmacological and therapeutic properties of ritonavir-boosted protease inhibitor therapy in HIV-infected patients. J Antimicrob Chemother. 2004; 53: 4-9. doi: 10.1093/jac/ dkh029 PMID: 14657084
47. Braeckman BP, Houthoofd K, Brys K, Lenaerts I, De Vreese A, Van Eygen S, et al. No reduction of energy metabolism in Clk mutants. Mech Ageing Dev. 2002/11/12 ed. 2002; 123: 1447-56. PMID: 12425951
48. Jonassen T, Larsen PL, Clarke CF. A dietary source of coenzyme Q is essential for growth of long-lived Caenorhabditis elegans clk-1 mutants. Proc Natl Acad Sci U S A. 2001; 98: 421-426. doi: 10.1073/ pnas.98.2.421 PMID: 11136229
49. De Vos WH, Van Neste L, Dieriks B, Joss GH, Van Oostveldt P. High content image cytometry in the context of subnuclear organization. Cytom Part A J Int Soc Anal Cytol. 2009/10/13 ed. 2010; 77: 64-75. doi: 10.1002/cyto.a.20807
50. Golden TR, Beckman KB, Lee AHJ, Dudek N, Hubbard A, Samper E, et al. Dramatic age-related changes in nuclear and genome copy number in the nematode Caenorhabditis elegans. Aging Cell. 2007; 6: 179-88. doi: 10.1111/j.1474-9726.2007.00273.x PMID: 17286610