The lampricide 3-trifluoromethyl-4-nitrophenol (TFM) uncouples mitochondrial oxidative phosphorylation in both sea lamprey (Petromyzon marinus) and TFM-tolerant rainbow trout (Oncorhynchus mykiss)

Birceanu, Oana; McClelland, Grant B.; Wang, Yuxiang S.; Brown, Jason C. L.; Wilkie, Michael P.

doi:10.1016/j.cbpc.2010.12.005

Cited by 37 publications

(54 citation statements)

References 52 publications

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“…Statistically significant differences from controls (no TFM) are denoted by asterisks. mitochondrial membrane, which separates the mitochondrial matrix from the intermembrane space (Birceanu et al 2011). A consequence of this uncoupling is a greater reliance on highenergy phosphagens such as PCr in fishes and phosphoarginine in molluscs (Viant et al 2001) to temporarily maintain the ATP supply and permit short-term survival (Hochachka 1991).…”

Section: Resilience Of Sea Lampreys To Tfmmentioning

confidence: 99%

“…Following 4-12 h of depuration in TFM-free water, these disturbances were readily reversed in the 80% of animals that survived TFM exposure. TFM impairs ATP production in the body by uncoupling oxidative phosphorylation (Niblett and Ballantyne 1976;Birceanu et al 2011). Like other uncouplers, TFM acts as a protonophore that leads to a dissipation of the proton electrochemical gradient (proton motive force) across the inner mitochondrial membrane, which separates the mitochondrial matrix from the intermembrane space (Birceanu et al 2011).…”

Section: Resilience Of Sea Lampreys To Tfmmentioning

confidence: 99%

“…TFM has been used to control sea lamprey populations in the Great Lakes since the 1960s (Lawrie 1970;Olson and Marking 1973;Smith and Tibbles 1980;McDonald and Kolar 2007;GLFC 2008). By interfering with the aerobic production of ATP in the mitochondria of cells (Niblett and Ballantyne 1976;Birceanu et al 2011), TFM causes death in sea lampreys by impairing energy supply, which ultimately leads to homeostatic disturbances in the body that cause death (Wilkie et al 2007;Birceanu et al 2009). The mechanism of toxicity is likely identical in nontarget fishes (Birceanu et al 2011), but it usually has minimal effects due to the greater capacity of nontarget fishes to detoxify TFM using phase II biotransformation in which TFM is converted to TFM-glucuronide in the liver (Lech and Statham 1975;Kane et al 1993).…”

mentioning

confidence: 99%

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Recovery of Larval Sea Lampreys from Short‐Term Exposure to the Pesticide 3‐Trifluoromethyl‐4‐Nitrophenol: Implications for Sea Lamprey Control in the Great Lakes

et al. 2012

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For over 50 years, invasive sea lamprey Petromyzon marinus populations have been controlled in the Great Lakes using the pesticide 3-trifluoromethyl-4-nitrophenol (TFM), which is applied to streams containing larval sea lampreys. The specificity of TFM is due to the sea lamprey's relative inability to detoxify it using glucuronidation; this inability causes death by interfering with the production of ATP, the main energy currency of cells. TFM treatments typically last 12 h, but given the sea lamprey's relative inability to detoxify TFM we predicted that TFM-induced homeostatic disturbances and toxicity would occur following shorter periods of exposure. Accordingly, we exposed larval sea lampreys to the 12-h LC99.9 (i.e., the concentration lethal to 99.9% of the test subjects over 12 h) of TFM for 4 or 6 h and monitored the survival and replenishment of energy stores and metabolite concentrations in surviving sea lampreys over a 24-h depuration period. Minimal mortality (∼20%) was observed during the post-TFM recovery, despite respective 50% and 70% reductions in brain and liver ATP, 70-90% decreases in brain phosphocreatine (PCr), and 30-50% reductions in brain and liver glycogen with corresponding increases in lactate. While relatively resistant to TFM, muscle still underwent a 55% decline in PCr. However, energy stores and metabolites returned to preexposure levels 4-12 h after TFM exposure. We conclude that sea lampreys can rapidly restore homeostasis following shorter-term TFM exposure. The resilience of sea lampreys to shorter-term TFM exposure suggests that there is no merit in reducing TFM treatment times from 12 h, which could lead to "treatment residuals" that survive lampricide treatments. This capacity to reverse TFM-induced perturbations also suggests that larvae seen emerging from the stream substrate late in a treatment, or that find refuge near streambanks or in isolated pools, could be another source of treatment residuals, leading to increased sea lamprey parasitism of sport and commercial fisheries in the Great Lakes.

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Section: Resilience Of Sea Lampreys To Tfmmentioning

confidence: 99%

Section: Resilience Of Sea Lampreys To Tfmmentioning

confidence: 99%

mentioning

confidence: 99%

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Recovery of Larval Sea Lampreys from Short‐Term Exposure to the Pesticide 3‐Trifluoromethyl‐4‐Nitrophenol: Implications for Sea Lamprey Control in the Great Lakes

et al. 2012

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“…Despite the frequent use of TFM as a measure to reduce sea lamprey populations and the reports of mostly sublethal nontarget species effects posttreatment, few studies have addressed potential molecular alterations resulting from TFM treatment. Growth was reduced dramatically when cells were forced to utilize aerobic respiration in the presence of TFM, which was expected because TFM is known to be a metabolic uncoupler of electron transport and ATP synthesis in the mitochondria . Perhaps more surprising were the impacts on growth and viability when yeast were grown in fermentable medium containing glucose, the preferred carbon source in yeast.…”

Section: Discussionmentioning

confidence: 99%

“…Similar to the classic uncoupling chemical 2,4‐dinitrophenol (DNP), TFM is a hydrophobic, phenolic weak acid that releases hydrogen ions in the mitochondrial matrix, disrupting the hydrogen ion gradient required to fuel adenosine 5′‐triphosphate (ATP) synthesis . Studies in rat mitochondria , trout , and sea lamprey larvae have shown that TFM uncouples oxidative phosphorylation from ATP synthesis, leading to ATP deficits, a reduction in glycogen reserves, and increased oxygen consumption.…”

Section: Introductionmentioning

confidence: 99%

Exposure to the lampricide 3‐trifluoromethyl‐4‐nitrophenol results in increased expression of carbohydrate transporters in Saccharomyces cerevisiae

Hinkle

Anderson

Forkey

et al. 2016

Enviro Toxic and Chemistry

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The lampricide 3-trifluoromethyl-4-nitrophenol (TFM) is used to control sea lamprey (Petromyzon marinus) populations in freshwater lakes. While TFM can have sublethal and lethal effects, little is known about gene expression changes with TFM exposure. Microarray analysis was used to determine differential gene expression over 4 hours of exposure in S. cerevisiae. Among the most significantly up regulated genes were regulators of carbohydrate transport including HXT1, HXT3, HXT4, IMA5, MIG2, and YKR075C.

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A Toxic Unit and Additive Index Approach to Understanding the Interactions of 2 Piscicides, 3‐Trifluoromethyl‐4‐Nitrophenol and Niclosamide, in Rainbow Trout

Hepditch

Birceanu

Wilkie

2021

Enviro Toxic and Chemistry

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The toxic unit and additive index approaches were used to understand how 2 pesticides, 3‐trifluoromethyl‐4‐nitrophenol (TFM) and 2,5‐dichloro‐4‐nitrosalicylanilide (niclosamide; Nic), interact in mixtures. Our first objective was to determine whether the interaction was strictly additive or greater than additive at doses comparable to those used to control invasive sea lamprey (Petromyzon marinus) in the Laurentian Great Lakes, and our second was to compare the utility of the toxic unit and additive index models for determining how TFM and Nic interacted. Typically, TFM is mixed with Nic (1–2%, w/v) to increase its potency and reduce TFM use. However, there is little information on how the 2 chemicals interact. Using a well‐studied, resident nontarget fish, the rainbow trout (Oncorhynchus mykiss), we conducted toxicity tests with TFM, Nic, and TFM:Nic (100:1, w/v; TFM/1% Nic) mixtures over 12 h to determine if the interaction was strictly additive, less than additive (antagonistic), or greater than additive (synergistic). The toxic unit and additive index approaches indicated synergistic interactions at environmentally relevant concentrations, suggesting that both are valid approaches for predicting how TFM and Nic interact. The toxic unit approach was simpler to conceptualize and to calculate, and we recommend that it be used when describing how TFM and Nic, and other similar organic compounds, interact with each other in aquatic ecosystems. Environ Toxicol Chem 2021;40:1419–1430. © 2021 The Authors. Environmental Toxicology and Chemistry published by Wiley Periodicals LLC on behalf of SETAC.

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The lampricide 3-trifluoromethyl-4-nitrophenol (TFM) uncouples mitochondrial oxidative phosphorylation in both sea lamprey (Petromyzon marinus) and TFM-tolerant rainbow trout (Oncorhynchus mykiss)

Cited by 37 publications

References 52 publications

Recovery of Larval Sea Lampreys from Short‐Term Exposure to the Pesticide 3‐Trifluoromethyl‐4‐Nitrophenol: Implications for Sea Lamprey Control in the Great Lakes

Recovery of Larval Sea Lampreys from Short‐Term Exposure to the Pesticide 3‐Trifluoromethyl‐4‐Nitrophenol: Implications for Sea Lamprey Control in the Great Lakes

Exposure to the lampricide 3‐trifluoromethyl‐4‐nitrophenol results in increased expression of carbohydrate transporters in Saccharomyces cerevisiae

A Toxic Unit and Additive Index Approach to Understanding the Interactions of 2 Piscicides, 3‐Trifluoromethyl‐4‐Nitrophenol and Niclosamide, in Rainbow Trout

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