Study of the relationship between thyroid hormones and lipid metabolism during KClO4-induced metamorphosis of landlocked lamprey, Petromyzon marinus

Abstract

This study examines the role of thyroid hormones (TH) (thyroxine and triiodothyronine) in regulating lipid metabolism of landlocked larval sea lampreys, Petromyzon marinus. Larvae were treated with either thyroxine (0.5 or 1 mg l − 1 water) or triiodothyronine (0.25 or 1 mg l − 1 water) in the presence or absence of the goitrogen, potassium perchlorate (KClO 4 ) (0.05% w/v), for 4, 8, and 16 weeks. Treatment with KClO 4 alone, which induced metamorphosis after 8 weeks and lowered plasma TH levels, reduced hepatic and renal total lipid content after 8 weeks of treatment. KClO 4 -induced lipid depletion after the 8-week treatment was supported by an increased rate of hepatic lipolysis, as indicated by increased triacylglycerol lipase activity. Furthermore, reduced lipogenesis in the liver was indicated by decreased hepatic acetyl-CoA carboxylase and diacylglycerol acyltransferase (DGAT) activities, and by decreased renal DGAT activity following 8 weeks of KClO 4 treatment. Treatment of larvae for 4 weeks with TH alone resulted in either no change or a slight increase of lipid in the liver and kidney. TH treatments in combination with KClO 4 failed to induce metamorphosis and, after up to 8 weeks, several TH treatments blocked changes in lipid content and enzyme activity associated with KClO 4 -induced metamorphosis. These experimental results suggest that TH deficiency during metamorphosis may promote lipid catabolism, while the presence of TH tends to protect/promote lipid reserves, perhaps favoring the larval condition. The actions of TH and KClO 4 on metamorphosis-associated lipid metabolism in sea lampreys may be direct, permissive, and/or indirect via other factors.

Deiodinases and thyroid metabolism disruption in teleost fish

“…In fish, thyroid metabolism plays a pivotal role in some development processes such as growth and Contents lists available at ScienceDirect journal homepage: www.elsevier.com/locate/envres maturation (Sower et al, 1985;Walpita et al, 2009), smoltification (Björnsson et al, 2011), osmoregulation (Peter, 2011) and larval metamorphosis (Klaren et al, 2008;Taillebois et al, 2011). Additionally, the thyroid system is involved in immune system development (Lam et al, 2005), regulation of the intermediate metabolism (Kao et al, 1999) and behavior patterns (Edeline et al, 2005;Imbert et al, 2008). Therefore, alterations in the thyroid metabolism may affect those processes, leading to physiological abnormalities and other adverse effects, which in turn may compromise the correct balance of populations and even species survival.…”

Triglyceride accumulation in injured renal tubular cells: Alterations in both synthetic and catabolic pathways

“…Triglycerides are primarily synthesized in liver, intestine, and adipocytes [1]. However, that acyl-coenzyme A:diacylglycerol acyltransferases (DGATs), the enzymes which catalyze the final step of triglyceride synthesis, are expressed in most tissues [10], including kidney [11], suggest the potential broad based relevance of this cytoprotective pathway.…”

Effect of Somatostatins and Insulin on Blood Glucose Levels of Larvae and Metamorphosing Landlocked Sea Lamprey, Petromyzon marinus

“…This notion is supported by the observation that TH deficiency, caused by treatment with goitrogens, induces precocious metamorphosis of four Northern Hemisphere lamprey species, Lampetra planeri (Hoheisel and Sterba, 1963), L. reissneri (Suzuki, 1986), P. marinus (Youson et al ., 1995), and L. appendix (Holmes et al ., 1999). In addition, TH treatment completely blocked KClO 4 -induced metamorphosis (Manzon et al ., 1998) and inhibited KClO 4 -induced changes in lipid metabolism that are similar to those observed during spontaneous metamorphosis (Kao et al ., 1999a). A recent report indicated that, with the exception of propylthiouracil, several different goitrogens (i.e., potassium thiocyanate, sodium perchlorate and methimazole) induced metamorphosis in P. marinus larvae (Manzon et al ., 2001).…”

“…Second, TH deficiency induces precocious metamorphosis of P. marinus (Youson et al ., 1995;Manzon et al ., 2001); whereas, TH treatment blocks KClO 4 -induced metamorphosis (Manzon et al ., 1998). Finally, alterations in plasma levels of INS and TH are spontaneously associated with lamprey metamorphosis (Youson et al ., 1994) and both hormones play an anabolic role in the metamorphosis-associated changes in lamprey lipid metabolism (Kao et al ., 1999a and1999b).…”