Atlantic hagfish cardiac muscle: metabolic basis of tolerance to anoxia

Abstract

Oxygen tensions in the major venous inputs to the systemic and portal-vein hearts of normoxic Atlantic hagfish (12.3 +/- 1.7 and 11.0 +/- 1.6 mmHg, respectively) are low compared with typical vertebrate values. Anoxia and poisoning with cyanide and azide do not significantly affect in situ performance of the systemic heart. Idoacetate poisoning, however, results in a significant decrease in cardiac performance of the systemic heart to 12% of the initial value after 3 h. Activities of mitochondrial enzymes of hagfish ventricle suggest a small potential for aerobic metabolism compared with those in the aerobic ventricle of Atlantic cod. Activities of enzymes of carbohydrate metabolism indicate similar anaerobic capacity in hagfish and cod ventricle. The ratio of pyruvate kinase to cytochrome c oxidase, an index of anaerobic to aerobic capacity, is 5.6 times greater in hagfish than cod ventricle. Metabolite concentrations in freeze-clamped ventricles of normoxic and hypoxic hagfish indicate hypoxia-induced activation of glycogenolysis, enhanced substrate flow across 6-phosphofructokinase, and an apparent secondary constriction of glycolysis at the level of glyceraldehyde-phosphate dehydrogenase. Carbohydrate utilization via the glycolytic pathway appears essential for maintenance of cardiac performance in both normoxic and anoxic hagfish. Under conditions of severe hypoxia, ATP provision is probably met by anaerobic glycolysis.

Introducing a novel mechanism to control heart rate in the ancestral pacific hagfish

“…This is done via modulation of catecholamine release from chromaffin tissue located within the cardiac chambers themselves (Euler and Fänge, 1961;Bloom et al, 1963;Perry et al, 1993;Axelsson et al, 1990;Farrell, 2007). A tonic β-adrenergic stimulation of the hagfish heart is consistent with the bradycardic effects of sotalol in vivo (Hansen and Sidell, 1983;Axelsson et al, 1990) and nadolol in vitro ( present study). Production and recycling of catecholamines involves the ratelimiting conversion of tyrosine to 3,4-dihydroxyphenylalanine, which requires oxygen (Levitt et al, 1965).…”

“…Beyond their basal position in vertebrate evolution, hagfishes are biologically intriguing because of their anoxia tolerance and their legendary ability to produce copious amounts of slime (Hansen and Sidell, 1983;Stecyk and Farrell, 2006;Cox et al, 2010;Herr et al, 2010). More recently, hagfish have been proposed as champions of CO 2 tolerance (Baker et al, 2015).…”

“…Immediately after normoxic conditions are restored, heart rate then increases to 17.5 beats min −1 , almost double the normoxic heart rate, and cardiac output increases. Thus, over a 1-h period when the hagfish heart switches from sustained anaerobic metabolism (Hansen and Sidell, 1983;Farrell and Stecyk, 2007;Cox et al, 2011) back to aerobic metabolism, heart rate quadruples (∼4 to 17 beats min −1 ; Cox et al, 2010). Therefore, it is surprising that the hagfish can regulate its heart rate over such a large range without any cardiac innervation.…”

In situcardiac performance of Pacific bluefin tuna hearts in response to acute temperature change

“…Crude homogenates were prepared and CS activity was determined by the reduction of 5,5′-dithiobis(2-nitrobenzoic acid) (DTNB) and the resulting change in absorbance at 412·nm using a Perkin-Elmer Lamda 6 spectrophotometer (Norwalk, CT, USA). The reaction mixture contained 0.4·mmol·l -1 acetyl CoA, 0.25·mmol·l -1 DTNB, 0.5·mmol·l -1 oxaloacetate and 50·mmol·l -1 imidazole, pH·7.83 (Hansen and Sidell, 1983). Reactions were conducted at 25°C.…”

Comparison of Two Jacuzzis and Swimming Mild Recoveries on Heart Beat Rate and Myocardial Oxygen Consumption of Swimming

“…By contrast, experimental evidence indicates that the hearts of teleost fish function aerobically (Driedzic, 1983;Driedzic et al 1983: Farrellefa, 1985. The anoxic tolerance of the heart of the Atlantic hagfish Myxine glutinosa has been demonstrated in vitro (Rybak and Boivinet, 1959), together with its dependence upon glycolysis for the supply of energy (Rybak, 1959;Hansen and Sidell, 1983). Recently it has been shown that M. glutinosa can maintain cardiac output in vivo T even during severe environmental hypoxia (Axelsson et al 1990).…”