Tetracyclines disturb mitochondrial function across eukaryotic models: A call for caution in biomedical research

Cell Reports

Volumn 10, Issue 10, 2015, Pages 1681-1691

  Moullan, Norman ^a   Mouchiroud, Laurent ^a   Wang, Xu ^a   Ryu, Dongryeol ^a   Williams, Evan G ^a   Mottis, Adrienne ^a   Jovaisaite, Virginija ^a   Frochaux, Michael V ^a   Quiros, Pedro M ^a   Deplancke, Bart ^a   Houtkooper, Riekelt H ^b   Auwerx, Johan ^a  

^a EPFL   (Switzerland)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

AMOXICILLIN; DOXYCYCLINE; MITOCHONDRIAL PROTEIN; MITONUCLEAR PROTEIN; TETRACYCLINE DERIVATIVE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BIOSAFETY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOTOXICITY; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG SAFETY; EMBRYO; FEMALE; GENE EXPRESSION; HAZARD ASSESSMENT; HUMAN; HUMAN CELL; MALE; MITOCHONDRIAL DYNAMICS; MOUSE; NONHUMAN; PLANT GROWTH; PRIORITY JOURNAL; PROTEIN HOMEOSTASIS;

EUKARYOTA; MUS; PROTEOBACTERIA;

EID: 84925152196     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.02.034     Document Type: Article

References (43)

1. Andreux P.A., Houtkooper R.H., Auwerx J. Pharmacological approaches to restore mitochondrial function. Nat. Rev. Drug Discov. 2013, 12:465-483.
2. Argmann C.A., Chambon P., Auwerx J. Mouse phenogenomics: the fast track to "systems metabolism". Cell Metab. 2005, 2:349-360.
3. Bowman S.M., Drzewiecki K.E., Mojica E.R., Zielinski A.M., Siegel A., Aga D.S., Berry J.O. Toxicity and reductions in intracellular calcium levels following uptake of a tetracycline antibiotic in Arabidopsis. Environ. Sci. Technol. 2011, 45:8958-8964.
4. Branda C.S., Dymecki S.M. Talking about a revolution: The impact of site-specific recombinases on genetic analyses in mice. Dev. Cell 2004, 6:7-28.
5. Brummett R.E., Fox K.E. Aminoglycoside-induced hearing loss in humans. Antimicrob. Agents Chemother. 1989, 33:797-800.
6. Cho I., Yamanishi S., Cox L., Methé B.A., Zavadil J., Li K., Gao Z., Mahana D., Raju K., Teitler I., et al. Antibiotics in early life alter the murine colonic microbiome and adiposity. Nature 2012, 488:621-626.
7. Clark-Walker G.D., Linnane A.W. Invivo differentiation of yeast cytoplasmic and mitochondrial protein synthesis with antibiotics. Biochem. Biophys. Res. Commun. 1966, 25:8-13.
8. Cole M., Elson S., Fullbrook P.D. Inhibition of the -lactamases of Escherichia coli and Klebsiella aerogenes by semi-synthetic penicillins. Biochem. J. 1972, 127:295-308.
9. Connolly M.A., Clausen P.A., Lazar J.G. Preparation of RNA from plant tissue using trizol. CSH Protoc 2006, 2006. 10.1101/pdb.prot4105.
10. Du X., Wang Q.R., Chan E., Merchant M., Liu J., French D., Ashkenazi A., Qing J. FGFR3 stimulates stearoyl CoA desaturase 1 activity to promote bladder tumor growth. Cancer Res. 2012, 72:5843-5855.
11. Durieux J., Wolff S., Dillin A. The cell-non-autonomous nature of electron transport chain-mediated longevity. Cell 2011, 144:79-91.
12. FDA (2011). Summary report on antimicrobials sold or distributed for use in food-producing animals. http://www.fda.gov/downloads/ForIndustry/UserFees/AnimalDrugUserFeeActADUFA/UCM338170.pdf.
13. Feil R., Brocard J., Mascrez B., LeMeur M., Metzger D., Chambon P. Ligand-activated site-specific recombination in mice. Proc. Natl. Acad. Sci. USA 1996, 93:10887-10890.
14. Gao A.W., Cantó C., Houtkooper R.H. Mitochondrial response tonutrient availability and its role in metabolic disease. EMBO Mol. Med. 2014, 6:580-589.
15. Gossen M., Bujard H. Tight control of gene expression in mammalian cells by tetracycline-responsive promoters. Proc. Natl. Acad. Sci. USA 1992, 89:5547-5551.
16. Gossen M., Freundlieb S., Bender G., Müller G., Hillen W., Bujard H. Transcriptional activation by tetracyclines in mammalian cells. Science 1995, 268:1766-1769.
17. Houtkooper R.H., Mouchiroud L., Ryu D., Moullan N., Katsyuba E., Knott G., Williams R.W., Auwerx J. Mitonuclear protein imbalance as a conserved longevity mechanism. Nature 2013, 497:451-457.
18. Hvistendahl M. Public health. China takes aim at rampant antibiotic resistance. Science 2012, 336:795.
19. Jacoby R.P., Li L., Huang S., Pong Lee C., Millar A.H., Taylor N.L. Mitochondrial composition, function and stress response in plants. J.Integr. Plant Biol. 2012, 54:887-906.
20. Jovaisaite V., Mouchiroud L., Auwerx J. The mitochondrial unfolded protein response, a conserved stress response pathway with implications in health and disease. J.Exp. Biol. 2014, 217:137-143.
21. Lagouge M., Argmann C., Gerhart-Hines Z., Meziane H., Lerin C., Daussin F., Messadeq N., Milne J., Lambert P., Elliott P., et al. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 2006, 127:1109-1122.
22. Lelliott C.J., López M., Curtis R.K., Parker N., Laudes M., Yeo G., Jimenez-Liñan M., Grosse J., Saha A.K., Wiggins D., et al. Transcript and metabolite analysis of the effects of tamoxifen in rat liver reveals inhibition of fatty acid synthesis in the presence of hepatic steatosis. FASEB J. 2005, 19:1108-1119.
23. Liesa M., Shirihai O.S. Mitochondrial dynamics in the regulation of nutrient utilization and energy expenditure. Cell Metab. 2013, 17:491-506.
24. Liu Z., Butow R.A. Mitochondrial retrograde signaling. Annu. Rev. Genet. 2006, 40:159-185.
25. López M., Lelliott C.J., Tovar S., Kimber W., Gallego R., Virtue S., Blount M., Vázquez M.J., Finer N., Powles T.J., et al. Tamoxifen-induced anorexia is associated with fatty acid synthase inhibition in the ventromedial nucleus of the hypothalamus and accumulation of malonyl-CoA. Diabetes 2006, 55:1327-1336.
26. Mathews S., Reinhold D. Biosolid-borne tetracyclines and sulfonamides in plants. Environ. Sci. Pollut. Res. Int. 2013, 20:4327-4338.
27. Minamino T., Gaussin V., DeMayo F.J., Schneider M.D. Inducible gene targeting in postnatal myocardium by cardiac-specific expression of a hormone-activated Cre fusion protein. Circ. Res. 2001, 88:587-592.
28. Mingeot-Leclercq M.P., Tulkens P.M. Aminoglycosides: nephrotoxicity. Antimicrob. Agents Chemother. 1999, 43:1003-1012.
29. Mouchiroud L., Houtkooper R.H., Moullan N., Katsyuba E., Ryu D., Cantó C., Mottis A., Jo Y.S., Viswanathan M., Schoonjans K., et al. The NAD(+)/Sirtuin Pathway Modulates Longevity through Activation of Mitochondrial UPR and FOXO Signaling. Cell 2013, 154:430-441.
30. No D., Yao T.P., Evans R.M. Ecdysone-inducible gene expression in mammalian cells and transgenic mice. Proc. Natl. Acad. Sci. USA 1996, 93:3346-3351.
31. Owusu-Ansah E., Song W., Perrimon N. Muscle mitohormesis promotes longevity via systemic repression of insulin signaling. Cell 2013, 155:699-712.
32. Ramot D., Johnson B.E., Berry T.L., Carnell L., Goodman M.B. The Parallel Worm Tracker: a platform for measuring average speed and drug-induced paralysis in nematodes. PLoS ONE 2008, 3:e2208.
33. Rhoads D.M., Subbaiah C.C. Mitochondrial retrograde regulation in plants. Mitochondrion 2007, 7:177-194.
34. Ryding A.D., Sharp M.G., Mullins J.J. Conditional transgenic technologies. J.Endocrinol. 2001, 171:1-14.
35. Schwarzländer M., Finkemeier I. Mitochondrial energy and redox signaling in plants. Antioxid. Redox Signal. 2013, 18:2122-2144.
36. Selimoglu E. Aminoglycoside-induced ototoxicity. Curr. Pharm. Des. 2007, 13:119-126.
37. Sew Y.S., Ströher E., Holzmann C., Huang S., Taylor N.L., Jordana X., Millar A.H. Multiplex micro-respiratory measurements of Arabidopsis tissues. New Phytol. 2013, 200:922-932.
38. Subramanian A., Tamayo P., Mootha V.K., Mukherjee S., Ebert B.L., Gillette M.A., Paulovich A., Pomeroy S.L., Golub T.R., Lander E.S., Mesirov J.P. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA 2005, 102:15545-15550.
39. Utomo A.R., Nikitin A.Y., Lee W.H. Temporal, spatial, and cell type-specific control of Cre-mediated DNA recombination in transgenic mice. Nat. Biotechnol. 1999, 17:1091-1096.
40. Van Aken O., Zhang B., Carrie C., Uggalla V., Paynter E., Giraud E., Whelan J. Defining the mitochondrial stress response in Arabidopsis thaliana. Mol. Plant 2009, 2:1310-1324.
41. Wetsel W.C., Mellon P.L., Weiner R.I., Negro-Vilar A. Metabolism of pro-luteinizing hormone-releasing hormone in immortalized hypothalamic neurons. Endocrinology 1991, 129:1584-1595.
42. Xie X., Zhou Q., Lin D., Guo J., Bao Y. Toxic effect of tetracycline exposure on growth, antioxidative and genetic indices of wheat (Triticum aestivum L.). Environ. Sci. Pollut. Res. Int. 2011, 18:566-575.
43. Youle R.J., van der Bliek A.M. Mitochondrial fission, fusion, and stress. Science 2012, 337:1062-1065.