Failure of ATP supply to match ATP demand: The mechanism of toxicity of the lampricide, 3-trifluoromethyl-4-nitrophenol (TFM), used to control sea lamprey (Petromyzon marinus) populations in the Great Lakes

Birceanu, Oana; McClelland, Grant B.; Wang, Yuxiang S.; Wilkie, Michael P.

doi:10.1016/j.aquatox.2009.07.012

Cited by 40 publications

(47 citation statements)

References 55 publications

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“…There were also marked differences in the resting glycogen concentrations reported by Birceanu et al (2009) and those in the present study, but brain glycogen concentrations are highly variable between different cohorts of sea lampreys (Rovainen et al 1969). We suggest that this and prolonged holding in the laboratory account for the brain glycogen concentration in the larval sea lampreys used by Birceanu et al (2009).…”

Section: Perturbation and Restoration Of High-energy Phosphagens And contrasting

confidence: 62%

“…As in Birceanu et al (2009), rapid and pronounced drops in brain glycogen were observed after 4 and 6 h of exposure to TFM, but levels were rapidly restored during the depuration period. There were also marked differences in the resting glycogen concentrations reported by Birceanu et al (2009) and those in the present study, but brain glycogen concentrations are highly variable between different cohorts of sea lampreys (Rovainen et al 1969).…”

Section: Perturbation and Restoration Of High-energy Phosphagens And mentioning

confidence: 87%

“…Each container was lined with approximately 2 g of diffusely distributed aquarium cotton to mimic the burrowing habitat and decrease metabolic stress to the animals (Birceanu et al 2009). The next morning, water flow was cut off to each chamber and sufficient amounts of TFM were added to yield a nominal TFM concentration equivalent to the 12-h LC99.9.…”

Section: Experimental Protocolmentioning

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: Perturbation and Restoration Of High-energy Phosphagens And contrasting

confidence: 62%

Section: Perturbation and Restoration Of High-energy Phosphagens And mentioning

confidence: 87%

Section: Experimental Protocolmentioning

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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“…Early speculation, based on studies from similarly structured compounds, was that TFM disrupts oxidative phosphorylation leading to rapid energy depletion (Applegate et al, 1966; Niblett and Ballantyne, 1976; Howell et al, 1980), but it was not until recently that this hypothesis was more definitively tested (Wilkie et al, 2007; Birceanu et al, 2009, 2011). Theoretically, if TFM disrupts oxidative phosphorylation, energy production would shift from the aerobic to anaerobic pathways, resulting in a decrease in glycogen and an increase in anaerobic waste products in tissues.…”

Section: The Sea Lamprey Invasion Of the Laurentian Great Lakesmentioning

confidence: 99%

“…Theoretically, if TFM disrupts oxidative phosphorylation, energy production would shift from the aerobic to anaerobic pathways, resulting in a decrease in glycogen and an increase in anaerobic waste products in tissues. Experiments showed that TFM exposure decreased glycogen concentrations in the brain, liver and muscle, while increasing lactate in the same tissues (Birceanu et al, 2009). These results support the hypothesis that TFM disrupts oxidative phosphorylation leading to a mismatch in energy supply and demand and a build-up of toxic anaerobic waste products ultimately leading to death.…”

Section: The Sea Lamprey Invasion Of the Laurentian Great Lakesmentioning

confidence: 99%

Use of physiological knowledge to control the invasive sea lamprey (Petromyzon marinus) in the Laurentian Great Lakes

Siefkes

2017

Conservation Physiology

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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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Failure of ATP supply to match ATP demand: The mechanism of toxicity of the lampricide, 3-trifluoromethyl-4-nitrophenol (TFM), used to control sea lamprey (Petromyzon marinus) populations in the Great Lakes

Cited by 40 publications

References 55 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

Use of physiological knowledge to control the invasive sea lamprey (Petromyzon marinus) in the Laurentian Great Lakes

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

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