Drug-Induced Mitochondrial Toxicity during Pregnancy
Diana Luz Juárez-Flores
Muscle Research and Mitochondrial Function Laboratory, Cellex-IDIBAPS, Faculty of Medicine and Health Sciences-University of Barcelona, Internal Medicine Department-Hospital Clínic of Barcelona (HCB), Barcelona, Spain
CIBERER, Madrid, Spain
Search for more papers by this authorAna Sandra Hernández
BCNatal—Barcelona Center for Maternal-Fetal and Neonatal Medicine (Hospital Clínic and Hospital Sant Joan de Deu), IDIBAPS, University of Barcelona, Barcelona, Spain
CIBERER, Madrid, Spain
Search for more papers by this authorLaura García-Otero
BCNatal—Barcelona Center for Maternal-Fetal and Neonatal Medicine (Hospital Clínic and Hospital Sant Joan de Deu), IDIBAPS, University of Barcelona, Barcelona, Spain
Search for more papers by this authorMariona Guitart-Mampel
Muscle Research and Mitochondrial Function Laboratory, Cellex-IDIBAPS, Faculty of Medicine and Health Sciences-University of Barcelona, Internal Medicine Department-Hospital Clínic of Barcelona (HCB), Barcelona, Spain
CIBERER, Madrid, Spain
Search for more papers by this authorMarc Catalán-García
Muscle Research and Mitochondrial Function Laboratory, Cellex-IDIBAPS, Faculty of Medicine and Health Sciences-University of Barcelona, Internal Medicine Department-Hospital Clínic of Barcelona (HCB), Barcelona, Spain
CIBERER, Madrid, Spain
Search for more papers by this authorIngrid González-Casacuberta
Muscle Research and Mitochondrial Function Laboratory, Cellex-IDIBAPS, Faculty of Medicine and Health Sciences-University of Barcelona, Internal Medicine Department-Hospital Clínic of Barcelona (HCB), Barcelona, Spain
CIBERER, Madrid, Spain
Search for more papers by this authorJose César Milisenda
Muscle Research and Mitochondrial Function Laboratory, Cellex-IDIBAPS, Faculty of Medicine and Health Sciences-University of Barcelona, Internal Medicine Department-Hospital Clínic of Barcelona (HCB), Barcelona, Spain
CIBERER, Madrid, Spain
Search for more papers by this authorJosep Maria Grau
Muscle Research and Mitochondrial Function Laboratory, Cellex-IDIBAPS, Faculty of Medicine and Health Sciences-University of Barcelona, Internal Medicine Department-Hospital Clínic of Barcelona (HCB), Barcelona, Spain
CIBERER, Madrid, Spain
Search for more papers by this authorFrancesc Cardellach
Muscle Research and Mitochondrial Function Laboratory, Cellex-IDIBAPS, Faculty of Medicine and Health Sciences-University of Barcelona, Internal Medicine Department-Hospital Clínic of Barcelona (HCB), Barcelona, Spain
CIBERER, Madrid, Spain
Search for more papers by this authorConstanza Morén
Muscle Research and Mitochondrial Function Laboratory, Cellex-IDIBAPS, Faculty of Medicine and Health Sciences-University of Barcelona, Internal Medicine Department-Hospital Clínic of Barcelona (HCB), Barcelona, Spain
CIBERER, Madrid, Spain
Search for more papers by this authorGlòria Garrabou
Muscle Research and Mitochondrial Function Laboratory, Cellex-IDIBAPS, Faculty of Medicine and Health Sciences-University of Barcelona, Internal Medicine Department-Hospital Clínic of Barcelona (HCB), Barcelona, Spain
CIBERER, Madrid, Spain
Search for more papers by this authorDiana Luz Juárez-Flores
Muscle Research and Mitochondrial Function Laboratory, Cellex-IDIBAPS, Faculty of Medicine and Health Sciences-University of Barcelona, Internal Medicine Department-Hospital Clínic of Barcelona (HCB), Barcelona, Spain
CIBERER, Madrid, Spain
Search for more papers by this authorAna Sandra Hernández
BCNatal—Barcelona Center for Maternal-Fetal and Neonatal Medicine (Hospital Clínic and Hospital Sant Joan de Deu), IDIBAPS, University of Barcelona, Barcelona, Spain
CIBERER, Madrid, Spain
Search for more papers by this authorLaura García-Otero
BCNatal—Barcelona Center for Maternal-Fetal and Neonatal Medicine (Hospital Clínic and Hospital Sant Joan de Deu), IDIBAPS, University of Barcelona, Barcelona, Spain
Search for more papers by this authorMariona Guitart-Mampel
Muscle Research and Mitochondrial Function Laboratory, Cellex-IDIBAPS, Faculty of Medicine and Health Sciences-University of Barcelona, Internal Medicine Department-Hospital Clínic of Barcelona (HCB), Barcelona, Spain
CIBERER, Madrid, Spain
Search for more papers by this authorMarc Catalán-García
Muscle Research and Mitochondrial Function Laboratory, Cellex-IDIBAPS, Faculty of Medicine and Health Sciences-University of Barcelona, Internal Medicine Department-Hospital Clínic of Barcelona (HCB), Barcelona, Spain
CIBERER, Madrid, Spain
Search for more papers by this authorIngrid González-Casacuberta
Muscle Research and Mitochondrial Function Laboratory, Cellex-IDIBAPS, Faculty of Medicine and Health Sciences-University of Barcelona, Internal Medicine Department-Hospital Clínic of Barcelona (HCB), Barcelona, Spain
CIBERER, Madrid, Spain
Search for more papers by this authorJose César Milisenda
Muscle Research and Mitochondrial Function Laboratory, Cellex-IDIBAPS, Faculty of Medicine and Health Sciences-University of Barcelona, Internal Medicine Department-Hospital Clínic of Barcelona (HCB), Barcelona, Spain
CIBERER, Madrid, Spain
Search for more papers by this authorJosep Maria Grau
Muscle Research and Mitochondrial Function Laboratory, Cellex-IDIBAPS, Faculty of Medicine and Health Sciences-University of Barcelona, Internal Medicine Department-Hospital Clínic of Barcelona (HCB), Barcelona, Spain
CIBERER, Madrid, Spain
Search for more papers by this authorFrancesc Cardellach
Muscle Research and Mitochondrial Function Laboratory, Cellex-IDIBAPS, Faculty of Medicine and Health Sciences-University of Barcelona, Internal Medicine Department-Hospital Clínic of Barcelona (HCB), Barcelona, Spain
CIBERER, Madrid, Spain
Search for more papers by this authorConstanza Morén
Muscle Research and Mitochondrial Function Laboratory, Cellex-IDIBAPS, Faculty of Medicine and Health Sciences-University of Barcelona, Internal Medicine Department-Hospital Clínic of Barcelona (HCB), Barcelona, Spain
CIBERER, Madrid, Spain
Search for more papers by this authorGlòria Garrabou
Muscle Research and Mitochondrial Function Laboratory, Cellex-IDIBAPS, Faculty of Medicine and Health Sciences-University of Barcelona, Internal Medicine Department-Hospital Clínic of Barcelona (HCB), Barcelona, Spain
CIBERER, Madrid, Spain
Search for more papers by this authorYvonne Will PhD, ATS Fellow
Pfizer Drug Safety R&D, Groton, CT, USA
Search for more papers by this authorSummary
In the context of pregnancy, mitochondrial toxicity may be manifested and exclusively restricted to the carrying mother (maternal toxicity) or may be translated into the embryo (fetal toxicity). This chapter describes the mechanisms of action and potential secondary mitochondrial effects of drugs currently used in clinical practice during pregnancy in an attempt to increase awareness and caution about their management. In case of human pregnancies, novel approaches based on in silico modeling and system pharmacology, aimed to design and predict on-target and off-target effects of a drug before administration, should be considered in order to maximize its therapeutic action and minimize its toxic consequences. During pregnancy, acute disorders, such as migraine or infectious diseases, may require short-term treatment with potential mitochondrial toxic medication. Although mitochondrial toxicity is widely documented in nonpregnant adults, little information is known within the context of human pregnancy, particularly in terms of in utero exposure.
References
-
Abdel-Razaq, W., Kendall, D.A. and Bates, T.E., 2011. The effects of antidepressants on mitochondrial function in a model cell system and isolated mitochondria. Neurochemical Research, 36(2), pp. 327–38.
10.1007/s11064-010-0331-z Google Scholar
- Aldrovandi, G.M. et al., 2009. Antiretroviral exposure and lymphocyte mtDNA content among uninfected infants of HIV-1-infected women. Pediatrics, 124(6), pp. e1189–97.
- Anderson, S., 1981. Sequence and organization of the human mitochondrial genome. Nature, 5806(290), pp. 457–65.
- Andrade, C., 2012. Selective serotonin reuptake inhibitors and persistent pulmonary hypertension of the newborn. The Journal of Clinical Psychiatry, 73(5), pp. e601–5.
- Andreu, A.L. and Gonzalo-Sanz, R., 2004. Mitochondrial disorders: a classification for the 21st century. Neurología (Barcelona, Spain), 19(1), pp. 15–22.
- Antonucci, R. et al., 2012. Use of non-steroidal anti-inflammatory drugs in pregnancy: impact on the fetus and newborn. Current Drug Metabolism, 13(4), pp. 474–90.
-
Artuch, R. et al., 2006. Cerebellar ataxia with coenzyme Q10 deficiency: diagnosis and follow-up after coenzyme Q10 supplementation. Journal of the Neurological Sciences, 246(1–2), pp. 153–8.
10.1016/j.jns.2006.01.021 Google Scholar
- Bai, J.P.F. et al., 2014. Systems pharmacology modeling: an approach to improving drug safety. Biopharmaceutics & Drug Disposition, 35(1), pp. 1–14.
-
Bar-Oz, B. et al., 2012. The outcomes of pregnancy in women exposed to the new macrolides in the first trimester. Drug Safety, 35(7), pp. 589–98.
10.2165/11630920-000000000-00000 Google Scholar
- Barker, D.J., 1999. Fetal origins of cardiovascular disease. Annals of Medicine, 31 Suppl 1, pp. 3–6.
- Barret, B. et al., 2003. Persistent mitochondrial dysfunction in HIV-1-exposed but uninfected infants: clinical screening in a large prospective cohort. AIDS (London, England), 17(12), pp. 1769–85.
- Battino, D. et al., 2013. Seizure control and treatment changes in pregnancy: observations from the EURAP epilepsy pregnancy registry. Epilepsia, 54(9), pp. 1621–7.
- Bérard, A. et al., 2015. Use of macrolides during pregnancy and the risk of birth defects: a population-based study. Pharmacoepidemiology and Drug Safety, 24(12), pp. 1241–8.
- Blohm, E., Lai, J. and Neavyn, M., 2017. Drug-induced hyperlactatemia. Clinical Toxicology, 55(8), pp. 869–78.
- Bressler, A.M. et al., 2004. Peripheral neuropathy associated with prolonged use of linezolid. The Lancet Infectious Diseases, 4(8), pp. 528–31.
- Brinkman, K. et al., 1998. Adverse effects of reverse transcriptase inhibitors: mitochondrial toxicity as common pathway. AIDS (London, England), 12(14), pp. 1735–44.
- Brinkman, K. et al., 1999. Mitochondrial toxicity induced by nucleoside-analogue reverse-transcriptase inhibitors is a key factor in the pathogenesis of antiretroviral-therapy-related lipodystrophy. Lancet (London, England), 354(9184), pp. 1112–5.
- Brocklehurst, P. and French, R., 1998. The association between maternal HIV infection and perinatal outcome: a systematic review of the literature and meta-analysis. British Journal of Obstetrics and Gynaecology, 105(8), pp. 836–48.
- Casademont, J. et al., 2007. Neuroleptic treatment effect on mitochondrial electron transport chain: peripheral blood mononuclear cells analysis in psychotic patients. Journal of Clinical Psychopharmacology, 27(3), pp. 284–8.
- Chen, S. et al., 2014. Sertraline, an antidepressant, induces apoptosis in hepatic cells through the mitogen-activated protein kinase pathway. Toxicological Sciences: An Official Journal of the Society of Toxicology, 137(2), pp. 404–15.
- Cherry, C.L. and Wesselingh, S.L., 2003. Nucleoside analogues and HIV: the combined cost to mitochondria. The Journal of Antimicrobial Chemotherapy, 51(5), pp. 1091–3.
- Contreras-Shannon, V. et al., 2013. Clozapine-induced mitochondria alterations and inflammation in brain and insulin-responsive cells. PLoS One, 8(3), p. e59012.
- Crispi, F. et al., 2010. Fetal growth restriction results in remodeled and less efficient hearts in children. Circulation, 121(22), pp. 2427–36.
- Curti, C. et al., 1999. Fluoxetine interacts with the lipid bilayer of the inner membrane in isolated rat brain mitochondria, inhibiting electron transport and F1F0-ATPase activity. Molecular and Cellular Biochemistry, 199(1–2), pp. 103–9.
- Davey, G.P., Peuchen, S. and Clark, J.B., 1998. Energy thresholds in brain mitochondria: potential involvement in neurodegeneration. Journal of Biological Chemistry, 273(21), pp. 12753–7.
- De Santis, M. et al., 2011. Antiepileptic drugs during pregnancy: pharmacokinetics and transplacental transfer. Current Pharmaceutical Biotechnology, 12(5), pp. 781–8.
-
Del Pozo, J.L. et al., 2014. Linezolid-induced lactic acidosis in two liver transplant patients with the mitochondrial DNA A2706G polymorphism. Antimicrobial Agents and Chemotherapy, 58(7), pp. 4227–9.
10.1128/AAC.02856-14 Google Scholar
- Estaquier, J. et al., 2002. Effects of antiretroviral drugs on human immunodeficiency virus type 1-induced CD4(+) T-cell death. Journal of Virology, 76(12), pp. 5966–73.
- Finsterer, J., 2009. Management of mitochondrial stroke-like-episodes. European Journal of Neurology: The Official Journal of the European Federation of Neurological Societies, 16(11), pp. 1178–84.
-
Finsterer, J., 2010. Treatment of mitochondrial disorders. European Journal of Paediatric Neurology: EJPN: Official Journal of the European Paediatric Neurology Society, 14(1), pp. 29–44.
10.1016/j.ejpn.2009.07.005 Google Scholar
- García-Otero, L. et al., 2016. Zidovudine treatment in HIV-infected pregnant women is associated with fetal cardiac remodelling. AIDS, 30(9), pp. 1393–401.
-
Garrabou, G. et al., 2009. Genetic and functional mitochondrial assessment of HIV-infected patients developing HAART-related hyperlactatemia. JAIDS Journal of Acquired Immune Deficiency Syndromes, 52(4), pp. 443–51.
10.1097/QAI.0b013e3181bd564c Google Scholar
- Garrabou, G. et al., 2011. Mitochondrial Pathophysiology, Transworld Research Network, pp. 249–79.
-
Gonçalves, V.F. et al., 2014. A hypothesis-driven association study of 28 nuclear-encoded mitochondrial genes with antipsychotic-induced weight gain in schizophrenia. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology, 39(6), pp. 1347–54.
10.1038/npp.2013.312 Google Scholar
- Gröber, U., 2012. Mitochondrial toxicity of drugs. Medizinische Monatsschrift für Pharmazeuten, 35(12), pp. 445–56.
- Guitart-Mampel, M. et al., 2017. Altered mitochondrial dynamics and apoptosis in HIV-pregnancies with obstetric complications. The Journal of Antimicrobial Chemotherapy, 72(9), pp. 2578–86.
- Guo, D. et al., 2010. The cardiotoxicity of macrolides: a systematic review. Die Pharmazie, 65(9), pp. 631–40.
- Guo, H. et al., 2017. Relationships between mitochondrial DNA content, mitochondrial activity, and boar sperm motility. Theriogenology, 87, pp. 276–83.
-
Haeri, S. et al., 2009. Obstetric and newborn infant outcomes in human immunodeficiency virus–infected women who receive highly active antiretroviral therapy. American Journal of Obstetrics and Gynecology, 201(3), pp. 315.e1–e5.
10.1016/j.ajog.2009.06.017 Google Scholar
- Hendrick, V. et al., 2003. Placental passage of antidepressant medications. American Journal of Psychiatry, 160(5), pp. 993–6.
- Hernandez, S. et al., 2016. Mitochondrial toxicity and caspase activation in HIV pregnant women. Journal of Cellular and Molecular Medicine, 21(1): 26–34.
-
Hernàndez, S. et al., 2012. Perinatal outcomes, mitochondrial toxicity and apoptosis in HIV-treated pregnant women and in-utero-exposed newborn. AIDS, 26(4), pp. 419–28.
10.1097/QAD.0b013e32834f3232 Google Scholar
-
Hernández, S. et al., 2017. Placental mitochondrial toxicity, oxidative stress, apoptosis, and adverse perinatal outcomes in HIV pregnancies under antiretroviral treatment containing zidovudine. JAIDS Journal of Acquired Immune Deficiency Syndromes, 75(4), pp. e113–9.
10.1097/QAI.0000000000001334 Google Scholar
- Herst, P.M. et al., 2017. Functional mitochondria in health and disease. Frontiers in Endocrinology, 8, p. 296.
- Hogan, Q. et al., 1994. Local anesthetic myotoxicity: a case and review. Anesthesiology, 80(4), pp. 942–7.
- Hong, S. et al., 2015. Evidence that antibiotics bind to human mitochondrial ribosomal RNA has implications for aminoglycoside toxicity. The Journal of Biological Chemistry, 290(31): 19273–86.
-
Hroudová, J. and Fišar, Z., 2012.
In vitro inhibition of mitochondrial respiratory rate by antidepressants. Toxicology Letters, 213(3), pp. 345–52.
10.1016/j.toxlet.2012.07.017 Google Scholar
- Jansen, R.P.S. and Burton, G.J., 2004. Mitochondrial dysfunction in reproduction. Mitochondrion, 4(5–6), pp. 577–600.
- Jao, J. and Abrams, E.J., 2014. Metabolic complications of in utero maternal HIV and antiretroviral exposure in HIV-exposed infants. The Pediatric Infectious Disease Journal, 33(7), pp. 734–40.
- Kieler, H. et al., 2011. Selective serotonin reuptake inhibitors during pregnancy and risk of persistent pulmonary hypertension in the newborn: population based cohort study from the five Nordic countries. BMJ, 344(jan12 3), pp. d8012–d8012.
-
Kirmse, B., Baumgart, S. and Rakhmanina, N., 2013. Metabolic and mitochondrial effects of antiretroviral drug exposure in pregnancy and postpartum: implications for fetal and future health. Seminars in Fetal and Neonatal Medicine, 18(1), pp. 48–55.
10.1016/j.siny.2012.10.005 Google Scholar
- Komulainen, T. et al., 2015. Sodium valproate induces mitochondrial respiration dysfunction in HepG2 in vitro cell model. Toxicology, 331, pp. 47–56.
-
Lambert, J.S. et al., 2000. Risk factors for preterm birth, low birth weight, and intrauterine growth retardation in infants born to HIV-infected pregnant women receiving zidovudine. Pediatric AIDS Clinical Trials Group 185 Team. AIDS (London, England), 14(10), pp. 1389–99.
10.1097/00002030-200007070-00012 Google Scholar
- Lang, B.F., Gray, M.W. and Burger, G., 1999. Mitochondrial genome evolution and the origin of eukaryotes. Annual Review of Genetics, 33(1), pp. 351–97.
-
Langs-Barlow, A. et al., 2015. Association of circulating cytochrome c with clinical manifestations of antiretroviral-induced toxicity. Mitochondrion, 20, pp. 71–4.
10.1016/j.mito.2014.11.004 Google Scholar
- Latini, R., Tognoni, G. and Kates, R.E., 1984. Clinical pharmacokinetics of amiodarone. Clinical Pharmacokinetics, 9(2), pp. 136–56.
-
Lee, M. et al., 2015. Tricyclic antidepressants amitriptyline and desipramine induced neurotoxicity associated with Parkinson's disease. Molecules and Cells, 38(8), pp. 734–40.
10.14348/molcells.2015.0131 Google Scholar
- Lewis, W. and Dalakas, M.C., 1995. Mitochondrial toxicity of antiviral drugs. Nature Medicine, 1(5), pp. 417–22.
-
Li, Y. et al., 2012. Mitochondrial dysfunction induced by sertraline, an antidepressant agent. Toxicological Sciences: An Official Journal of the Society of Toxicology, 127(2), pp. 582–91.
10.1093/toxsci/kfs100 Google Scholar
-
Lin, K.J. et al., 2013. Safety of macrolides during pregnancy. American Journal of Obstetrics and Gynecology, 208(3), pp. 221.e1–8.
10.1016/j.ajog.2012.12.023 Google Scholar
- López, S. et al., 2008. Mitochondrial DNA depletion in oocytes of HIV-infected antiretroviral-treated infertile women. Antiviral Therapy, 13(6), pp. 833–8.
- Mallal, S.A. et al., 2000. Contribution of nucleoside analogue reverse transcriptase inhibitors to subcutaneous fat wasting in patients with HIV infection. AIDS (London, England), 14(10), pp. 1309–16.
-
Mando, C. et al., 2014. Placental mitochondrial content and function in intrauterine growth restriction and preeclampsia. AJP: Endocrinology and Metabolism, 306(4), pp. E404–13.
10.1152/ajpendo.00426.2013 Google Scholar
- Margulis, L., 1975. Symbiotic theory of the origin of eukaryotic organelles; criteria for proof. Symposia of the Society for Experimental Biology, ( 29), pp. 21–38.
-
Martins, M.R. et al., 2008. Antipsychotic-induced oxidative stress in rat brain. Neurotoxicity Research, 13(1), pp. 63–9.
10.1007/BF03033368 Google Scholar
- Matsui, H. et al., 2011. The pathophysiology of non-steroidal anti-inflammatory drug (NSAID)-induced mucosal injuries in stomach and small intestine. Journal of Clinical Biochemistry and Nutrition, 48(2), pp. 107–11.
- Maurer, I. and Möller, H.J., 1997. Inhibition of complex I by neuroleptics in normal human brain cortex parallels the extrapyramidal toxicity of neuroleptics. Molecular and Cellular Biochemistry, 174(1–2), pp. 255–9.
- Monteiro, J.P. et al., 2014. Mitochondrial membrane lipids in life and death and their molecular modulation by diet: tuning the furnace. Current Drug Targets, 15(8), pp. 797–810.
-
Morén, C. et al., 2014. Mitochondrial toxicity in human pregnancy: an update on clinical and experimental approaches in the last 10 years. International Journal of Environmental Research and Public Health, 11(9), pp. 9897–918.
10.3390/ijerph110909897 Google Scholar
- Morén, C. et al., 2015. Mitochondrial disturbances in HIV pregnancies. AIDS, 29(1), pp. 5–12.
- Morén, C. et al., 2016. The role of therapeutic drugs on acquired mitochondrial toxicity. Current Drug Metabolism, 17(999), pp. 1–1.
- Mouton, J.P., Cohen, K. and Maartens, G., 2016. Key toxicity issues with the WHO-recommended first-line antiretroviral therapy regimen. Expert review of clinical pharmacology, 9(11), pp. 1493–503.
- Mussini, C. et al., 2005. Effect of treatment interruption monitored by CD4 cell count on mitochondrial DNA content in HIV-infected patients: a prospective study. AIDS (London, England), 19(15), pp. 1627–33.
- Nahon, E. et al., 2005. Fluoxetine (Prozac) interaction with the mitochondrial voltage-dependent anion channel and protection against apoptotic cell death. FEBS Letters, 579(22), pp. 5105–10.
-
Nau, H. et al., 1981. Thiamphenicol during the first trimester of human pregnancy: placental transfer in vivo, placental uptake in vitro, and inhibition of mitochondrial function. Toxicology and Applied Pharmacology, 60(1), pp. 131–41.
10.1016/0041-008X(81)90143-5 Google Scholar
- Negredo, E. et al., 2009. Improvement of mitochondrial toxicity in patients receiving a nucleoside reverse-transcriptase inhibitor-sparing strategy: results from the Multicenter Study with Nevirapine and Kaletra (MULTINEKA). Clinical Infectious Diseases: An Official Publication of the Infectious Diseases Society of America, 49(6), pp. 892–900.
- Negredo, E. et al., 2010. Mild improvement in mitochondrial function after a 3-year antiretroviral treatment interruption despite persistent impairment of mitochondrial DNA content. Current HIV Research, 8(5), pp. 379–85.
-
Noguera-Julian, A. et al., 2015. Decreased mitochondrial function among healthy infants exposed to antiretrovirals during gestation, delivery and the neonatal period. The Pediatric Infectious Disease Journal, 34(12), pp. 1349–54.
10.1097/INF.0000000000000894 Google Scholar
-
Nouette-Gaulain, K. et al., 2011. From analgesia to myopathy: when local anesthetics impair the mitochondrion. The International Journal of Biochemistry & Cell Biology, 43(1), pp. 14–9.
10.1016/j.biocel.2010.10.005 Google Scholar
- Nunnari, J. et al., 2012. Mitochondria: in sickness and in health. Cell, 148(6), pp. 1145–59.
- Opii, W.O. et al., 2007. Oxidative stress and toxicity induced by the nucleoside reverse transcriptase inhibitor (NRTI)—2′,3′-dideoxycytidine (ddC): relevance to HIV-dementia. Experimental Neurology, 204(1), pp. 29–38.
- Ornoy, A., 2009. Valproic acid in pregnancy: how much are we endangering the embryo and fetus? Reproductive Toxicology, 28(1), pp. 1–10.
-
Pacifici, G.M., 2005. Transfer of antivirals across the human placenta. Early Human Development, 81(8), pp. 647–54.
10.1016/j.earlhumdev.2005.02.002 Google Scholar
- Pacifici, G.M., 2006. Placental transfer of antibiotics administered to the mother: a review. International Journal of Clinical Pharmacology and Therapeutics, 44(2), pp. 57–63.
-
Pedrol, E. et al., 2005. Treatment of symptomatic hyperlactatemia and lactic acidosis in HIV+ patients under nucleoside reverse transcriptase inhibitors. Medicina Clínica, 125(6), pp. 201–4.
10.1157/13077376 Google Scholar
-
Petit, F. et al., 2005. Mitochondria are sensors for HIV drugs. Trends in Pharmacological Sciences, 26(5), pp. 258–64.
10.1016/j.tips.2005.03.006 Google Scholar
- Phenix, B.N. et al., 2001. Antiapoptotic mechanism of HIV protease inhibitors: preventing mitochondrial transmembrane potential loss. Blood, 98(4), pp. 1078–85.
-
Poirier, M.C. et al., 2003. Long-term mitochondrial toxicity in HIV-uninfected infants born to HIV-infected mothers. Journal of Acquired Immune Deficiency Syndromes (1999), 33(2), pp. 175–83.
10.1097/00126334-200306010-00010 Google Scholar
- Poirier, M.C. et al., 2015. Fetal consequences of maternal antiretroviral nucleoside reverse transcriptase inhibitor use in human and nonhuman primate pregnancy. Current Opinion in Pediatrics, 27(2), pp. 233–9.
- Pon, L.A. and Schon, E.A., 2007. Mitochondria, 2nd ed., San Diego, CA: Elsevier.
- Przedborski, S. et al., 1992. Transgenic mice with increased Cu/Zn-superoxide dismutase activity are resistant to N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced neurotoxicity. The Journal of Neuroscience: The Official Journal of the Society for Neuroscience, 12(5), pp. 1658–67.
- Raudenska, M. et al., 2013. Haloperidol cytotoxicity and its relation to oxidative stress. Mini Reviews in Medicinal Chemistry, 13(14), pp. 1993–8.
- Reynier, P. et al., 2001. Mitochondrial DNA content affects the fertilizability of human oocytes. Molecular Human Reproduction, 7(5), pp. 425–9.
-
Riggin, L. et al., 2013. The fetal safety of fluoxetine: a systematic review and meta-analysis. Journal of Obstetrics and Gynaecology Canada, 35(4), pp. 362–9.
10.1016/S1701-2163(15)30965-8 Google Scholar
- Rodriguez, R.J. and Acosta, D., 1996. Inhibition of mitochondrial function in isolated rate liver mitochondria by azole antifungals. Journal of Biochemical Toxicology, 11(3), pp. 127–31.
- Ross, A.C. et al., 2012. Effects of in utero antiretroviral exposure on mitochondrial DNA levels, mitochondrial function and oxidative stress. HIV Medicine, 13(2), pp. 98–106.
- Rudin, C. et al., 2011. Antiretroviral therapy during pregnancy and premature birth: analysis of Swiss data. HIV Medicine, 12(4), pp. 228–35.
- Rumbach, L. et al., 1986. Effects of sodium valproate on mitochondrial membranes: electron paramagnetic resonance and transmembrane protein movement studies. Molecular Pharmacology, 30(3), pp. 270–3.
- Salimi, A. et al., 2016. Toxicity of macrolide antibiotics on isolated heart mitochondria: a justification for their cardiotoxic adverse effect. Xenobiotica; The Fate of Foreign Compounds in Biological Systems, 46(1), pp. 82–93.
- Santos, N.A.G. et al., 2008. Aromatic antiepileptic drugs and mitochondrial toxicity: effects on mitochondria isolated from rat liver. Toxicology in Vitro: An International Journal Published in Association with BIBRA, 22(5), pp. 1143–52.
- Santos, T.A., El Shourbagy, S. and St. John, J.C., 2006. Mitochondrial content reflects oocyte variability and fertilization outcome. Fertility and Sterility, 85(3), pp. 584–91.
-
Scatena, R. et al., 2007. The role of mitochondria in pharmacotoxicology: a reevaluation of an old, newly emerging topic. American Journal of Physiology. Cell Physiology, 293(1), pp. C12–21.
10.1152/ajpcell.00314.2006 Google Scholar
- Scheffler, I.E., 2008. Mitochondria, 2nd ed., Hoboken, NJ: Wiley-Liss.
-
Shiramizu, B. et al., 2003. Placenta and cord blood mitochondrial DNA toxicity in HIV-infected women receiving nucleoside reverse transcriptase inhibitors during pregnancy. Journal of Acquired Immune Deficiency Syndromes (1999), 32(4), pp. 370–4.
10.1097/00126334-200304010-00004 Google Scholar
- Silva, M.F.B. et al., 2008. Valproic acid metabolism and its effects on mitochondrial fatty acid oxidation: a review. Journal of Inherited Metabolic Disease, 31(2), pp. 205–16.
- Singh, K.P., Singh, M.K. and Gautam, S., 2016. Effect of in utero exposure to the atypical anti-psychotic risperidone on histopathological features of the rat placenta. International Journal of Experimental Pathology, 97(2), pp. 125–32.
- Spaniol, M. et al., 2001. Toxicity of amiodarone and amiodarone analogues on isolated rat liver mitochondria. Journal of Hepatology, 35(5), pp. 628–36.
- Stewart, J.B. and Chinnery, P.F., 2015. The dynamics of mitochondrial DNA heteroplasmy: implications for human health and disease. Nature Reviews Genetics, 16(9), pp. 530– 42.
- Suy, A. et al., 2006. Increased risk of pre-eclampsia and fetal death in HIV-infected pregnant women receiving highly active antiretroviral therapy. AIDS (London, England), 20(1), pp. 59–66.
- Szewczyk, A. and Wojtczak, L., 2002. Mitochondria as a pharmacological target. Pharmacological Reviews, 54(1), pp. 101–27.
- Taylor, R.W. and Turnbull, D.M., 2005. Mitochondrial DNA mutations in human disease. Nature Reviews Genetics, 6(5), pp. 389–402.
- Thorne, C., Patel, D. and Newell, M.-L., 2004. Increased risk of adverse pregnancy outcomes in HIV-infected women treated with highly active antiretroviral therapy in Europe. AIDS (London, England), 18(17), pp. 2337–9.
- Timpka, S. et al., 2016. Hypertensive disorders of pregnancy and offspring cardiac structure and function in adolescence. Journal of the American Heart Association, 5(11), p. e003906.
- Tomson, T. et al., 2011. Dose-dependent risk of malformations with antiepileptic drugs: an analysis of data from the EURAP epilepsy and pregnancy registry. The Lancet Neurology, 10(7), pp. 609–17.
- Torres-Ruíz, N.M., Granados, O. and Meza, G., 2011. Aminoglycosides: therapeutics, ototoxicity and hypersensitivity of mitochondrial genetic origin. Proceedings of the Western Pharmacology Society, 54, pp. 49–51.
- Townsend, C.L. et al., 2007. Antiretroviral therapy and premature delivery in diagnosed HIV-infected women in the United Kingdom and Ireland. AIDS, 21(8), pp. 1019–26.
- Tuccori, M. et al., 2009. Safety concerns associated with the use of serotonin reuptake inhibitors and other serotonergic/noradrenergic antidepressants during pregnancy: a review. Clinical Therapeutics, 31, pp. 1426–53.
- Tuomala, R.E. et al., 2005. Improved obstetric outcomes and few maternal toxicities are associated with antiretroviral therapy, including highly active antiretroviral therapy during pregnancy. Journal of Acquired Immune Deficiency Syndromes (1999), 38(4), pp. 449–73.
-
Viora, M. et al., 1997. Interference with cell cycle progression and induction of apoptosis by dideoxynucleoside analogs. International Journal of Immunopharmacology, 19(6), pp. 311–21.
10.1016/S0192-0561(97)00041-6 Google Scholar
- Wallace, D.C. and Melov, S., 1998. Radicals r'aging. Nature Genetics, 19(2), pp. 105–6.
- Zhang, Y. et al., 1990. The oxidative inactivation of mitochondrial electron transport chain components and ATPase. The Journal of Biological Chemistry, 265(27), pp. 16330–6.