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PubMed2005

Calcium and protein phosphatase 1/2A attenuate N-methyl-D-aspartate receptor activity in the anoxic turtle cortex.

Excitotoxic cell death (ECD) is characteristic of mammalian brain following min of anoxia, but is not observed in the western painted turtle following days to months without oxygen. A key event in ECD is a massive increase in intracellular Ca(2+) by over-stimulation of N-methyl-d-aspartate receptors (NMDARs). The turtle's anoxia tolerance may involve the prevention of ECD by attenuating NMDAR-induced Ca(2+) influx. The goal of this study was to determine if protein phosphatases (PPs) and intracellular calcium mediate reductions in turtle cortical neuron whole-cell NMDAR currents during anoxia, thereby preventing ECD. Whole-cell NMDAR currents did not change during 80 min of normoxia, but decreased 56% during 40 min of anoxia. Okadaic acid and calyculin A, inhibitors of serine/threonine PP1 and PP2A, potentiated NMDAR currents during normoxia and prevented anoxia-mediated attenuation of NMDAR currents. Decreases in NMDAR activity during anoxia were also abolished by inclusion of the Ca(2+) chelator -- BAPTA and the calmodulin inhibitor -- calmidazolium. However, cypermethrin, an inhibitor of the Ca(2+)/calmodulin-dependent PP2B (calcineurin), abolished the anoxic decrease in NMDAR activity at 20, but not 40 min suggesting that this phosphatase might play an early role in attenuating NMDAR activity during anoxia. Our results show that PPs, Ca(2+) and calmodulin play an important role in decreasing NMDAR activity during anoxia in the turtle cortex. We offer a novel mechanism describing this attenuation in which PP1 and 2A dephosphorylate the NMDAR (NR1 subunit) followed by calmodulin binding, a subsequent dissociation of alpha-actinin-2 from the NR1 subunit, and a decrease in NMDAR activity.

Animals↗
PubMed2006

Lactate uptake by skeletal bone in anoxic turtles, Trachemys scripta.

Previous studies have shown that freshwater turtle shells can accumulate lactate during periods of anoxic submergence. Our objective in this study was to determine lactate uptake in other parts of the turtle's skeleton. We measured lactate concentration of 7 skeletal elements and 4 shell samples of red-eared slider turtles, Trachemys scripta, in control animals (N=12) and in animals following submergence for 4-5 days in N(2)-equilibrated water at 10 degrees C (N=8). We also collected blood samples and measured blood pH, PCO(2), and PO(2), and plasma lactate. Contralateral bone samples from 6 control turtles were analyzed for % water and mineral composition; bone from the other 6 were equilibrated with lactate solution in vitro. Anoxic submergence resulted in a combined respiratory/non-respiratory (lactic) acidosis and plasma lactate of 45.6+/-2.5 mmol l(-1). Shell and skeletal lactates all increased significantly in the anoxic animals (30.1-43.9 mmol kg(-1)) with limb bones having the highest levels and skull the least. Skeletal samples equilibrated in lactate solution in vitro for 2 days accumulated lactate in similar fashion with limb bones, except for fibula, higher, and skull significantly less than other bones. We conclude that the entire skeleton of the red-eared slider, like its shell, sequesters lactate and contributes thereby to lactic acid buffering.

Acidosis, Respiratory↗
PubMed2004

Effects of hibernation on mitochondrial regulation and metabolic capacities in myocardium of painted turtle (Chrysemys picta).

Painted turtles hibernating during winter may endure long-term exposure to low temperature and anoxia. These two conditions may affect the aerobic capacity of a tissue and might be of particular importance to the cardiac muscle normally highly reliant on aerobic energy production. The present study addressed how hibernation affects respiratory characteristics of mitochondria in situ and the metabolic pattern of turtle myocardium. Painted turtles were acclimated to control (25 degrees C), cold (5 degrees C) normoxic and cold anoxic conditions. In saponin-skinned myocardial fibres, cold acclimation increased mitochondrial respiratory capacity and decreased apparent ADP-affinity. Concomitant anoxia did not affect this. Creatine increased the apparent ADP-affinity to similar values in the three acclimation groups, suggesting a functional coupling of creatine kinase to mitochondrial respiration. As to the metabolic pattern, cold acclimation decreased glycolytic capacity in terms of pyruvate kinase activity and increased lactate dehydrogenase (LHD) activity. Concomitant anoxia counteracted the cold-induced decrease in pyruvate kinase activity and increased creatine kinase activity. In conclusion, cold acclimation seems to increase aerobic and decrease anaerobic energy production capacity in painted turtle myocardium. Importantly, anoxia does not affect the mitochondrial functional integrity but seems to increase the capacity for anaerobic energy production and energy buffering.

Adenosine Diphosphate↗
PubMed2005

Trace element (Cd, Cu, Hg, Se, Zn) accumulation and tissue distribution in loggerhead turtles (Caretta caretta) from the Western Mediterranean Sea (southern Italy).

Cadmium (Cd), copper (Cu), mercury (Hg), selenium (Se) and zinc (Zn) were determined in the liver, kidney and muscle of 29 loggerhead turtles, Caretta caretta, from the South Tyrrhenian Sea (Western Mediterranean). No significant differences (p>0.05) were detected between males and females. Trace element concentrations were not influenced by the size of the specimen except Se in the liver, which was negatively correlated with the curved carapace length (p<0.001). Muscles generally displayed the lowest trace element burdens, with the exception of Zn which contained concentrations as high as 176 microgg-1dwt. Kidneys displayed the highest Cd and Se mean concentrations (57.2+/-34.6 and 15.5+/-9.1 microgg-1dwt, respectively), while liver exhibited the highest Cu and Hg levels (37.3+/-8.7 and 1.1+/-1.7 microgg-1dwt, respectively). Whichever tissue is considered, the toxic elements had elevated coefficients of variation (i.e. from 60% to 177%) compared to those of the essential ones (i.e. from 14% to 65%), which is a consequence of homeostatic processes for Cu, Se and Zn. Globally, the concentrations of Hg remained low in all the considered tissues, possibly the result of low trophic level in sea turtles. In contrast, the diet of loggerhead turtles would result in a significant exposure to Cd. Highly significant correlations between Cd and Cu and Zn in the liver and kidney suggest that efficient detoxification processes involving MT occur which prevent Cd toxicity in loggerhead turtles.

Animals↗
PubMed2006

Phenotypically linked dichotomy in sea turtle foraging requires multiple conservation approaches.

Marine turtles undergo dramatic ontogenic changes in body size and behavior, with the loggerhead sea turtle, Caretta caretta, typically switching from an initial oceanic juvenile stage to one in the neritic, where maturation is reached and breeding migrations are subsequently undertaken every 2-3 years. Using satellite tracking, we investigated the migratory movements of adult females from one of the world's largest nesting aggregations at Cape Verde, West Africa. In direct contrast with the accepted life-history model for this species, results reveal two distinct adult foraging strategies that appear to be linked to body size. The larger turtles (n = 3) foraged in coastal waters, whereas smaller individuals (n = 7) foraged oceanically. The conservation implications of these findings are profound, with the population compartmentalized into habitats that may be differentially impacted by fishery threats in what is a global fishing hotspot. Although the protection of discrete areas containing coastal individuals may be attainable, the more numerous pelagic individuals are widely dispersed with individuals roaming over more than half a million square kilometers. Therefore, mitigation of fisheries by-catch for sea turtles in the east Atlantic will likely require complex and regionally tailored actions to account for this dichotomous behavior.

Africa, Western↗
PubMed2006

Loggerhead sea turtle (Caretta caretta) egg yolk concentrations of persistent organic pollutants and lipid increase during the last stage of embryonic development.

Data are scarce describing the concentrations of polychlorinated biphenyls (PCBs) and organochlorine pesticides in sea turtle eggs. The purpose of this study was to establish appropriate sample collection methodology to monitor these contaminants in sea turtle eggs. Contaminant concentrations were measured in yolk samples from eggs that failed to hatch from three loggerhead sea turtle (Caretta caretta) nests collected in southern Florida to determine if concentrations change through embryonic development. One to three egg yolk samples per nest were analyzed from early, middle, and late developmental stages (n=22 eggs total). PCB and pesticide concentrations were determined by gas chromatography with electron capture detection (GC-ECD). Geometric mean concentrations of summation operatorPCBs (52 congeners), summation operatorDDTs, summation operatorchlordanes, and dieldrin in all eggs were 65.0 (range=7.11 to 3930 ng/g lipid), 67.1 (range=7.88 to 1340 ng/g lipid), 37.0 (range=4.04 to 685 ng/g lipid), and 11.1 ng/g lipid (range=1.69 to 44.0 ng/g lipid), respectively. Early and middle developmental stage samples had similar concentrations of PCBs and organochlorine pesticides on a wet-mass basis (ng/g tissue extracted), but the concentrations doubled by the late stage. This increase is most likely attributable to the 50% increase in lipid content observed in the late-stage yolk. These findings indicate that an early-stage sample cannot be directly compared to a late-stage sample, especially from different nests. These preliminary findings also allowed us to calculate the minimum number of eggs per nest required for analysis to obtain an acceptable mean concentration per nest. More research is required to investigate geographical trends of contaminant concentrations and potential health effects (i.e., abnormalities) caused by these contaminants on sea turtle development.

Animals↗
PubMed2005

Mitogen-induced lymphocyte proliferation in loggerhead sea turtles: comparison of methods and effects of gender, plasma testosterone concentration, and body condition on immunity.

A fully functioning immune system is vital to the survival of threatened and endangered sea turtles. Immunological protection against diseases in any organism can be reduced by a number of natural and anthropogenic factors, such as seasonal changes, malnutrition, disease states, and contaminant exposure. These factors are even more critical when they occur in endangered species or populations. To identify alterations in the immunological health of loggerhead sea turtles (Caretta caretta), the mitogen-induced lymphocyte proliferation (LP) assay was developed using peripheral blood leukocytes (PBLs). Collection and culture conditions were optimized for this assay using non-lethal blood samples collected from free-ranging turtles along the southeastern US coast. During the collection, two anticoagulants (sodium heparin and lithium heparin) were compared to determine effects of different ions on assay results. Optimal culture conditions were established for loggerhead PBLs while two different methods of measuring LP were compared: (1) the traditional radioactive (3)H-thymidine assay and (2) a non-radioactive, colorimetric method utilizing 3-[4,5-dimethylthiazol-2-yl]-2,5-diphenyl tetrazolium (MTT). The results indicate that the (3)H-thymidine and the non-radioactive MTT methods did not correlate with each other and that the use of heparin type did not influence the results of the LP assay. Lastly, using these optimized methods, we investigated the effect of gender, plasma testosterone concentration, and body condition on LP in loggerhead turtles and found that none of the parameters largely influenced LP.

Animals↗
PubMed1997

Release of adenosine and ATP in the brain of the freshwater turtle (Trachemys scripta) during long-term anoxia.

Extracellular adenosine and ATP levels were monitored by microdialysis in the striatum of the freshwater turtle Trachemys scripta during long-term N2 respiration. After an initial rise in extracellular adenosine, a second peak of longer duration and higher in intensity, followed. The frequencies of these adenosine cycles varied considerably between individual turtles, such that the shortest time between the peaks was 80 min and the longest was 300 min (mean 151 min). After about 60 min anoxia, there was also a slow increase in extracellular ATP, rising from a normoxic concentration of 1.21 +/- 0.12 to 7.58 +/- 3.70 nmol l(-1) at 240 min anoxia. The results suggest that adenosine may continue to have a protective function in the turtle brain during long-term anoxia and that extracellular ATP might not function as an excitatory neurotransmitter in the anoxic turtle brain.

Adenosine↗
PubMed2003

Molecular cloning of proopiomelanocortin (POMC) cDNA from mud turtle, Pelodiscus sinensis.

The complete complementary DNA (cDNA) of proopiomelanocortin (POMC), a common precursor of opioid hormone beta-endorphin, melanotropin (MSH), and corticortropin (ACTH), was cloned and sequenced from pituitary and hypothalamus of mud turtle (Pelodiscus sinensis) by RT-PCR and rapid amplification of cDNA end (RACE) methods. Two transcripts of POMC mRNAs with different polyadenylation sites were observed. Both transcripts had an open reading frame encoding a 261-amino acid peptide containing nine dibasic amino acids (pair of Arg and Lys), putative proteolytic cleavage sites for processing to functional peptides. All the functional peptide fragments of mud turtle POMC, gamma-MSH, alpha-MSH, ACTH, beta-MSH, and beta-endorphin, are flanked by dibasic residues as found in other tetrapods, implying that it could be processed to give rise to all members of POMC-derived peptides. The deduced amino acid sequences of mud turtle POMC displays 63-67% identity with amphibian, 59% with chicken, 48-53% with mammals, and 37-59% identity with fish. However, functional peptide fragments are much more conserved than overall sequence and intervening fragments. In addition to pituitary and brain, mud turtle POMC mRNAs are also expressed in many peripheral tissues, such as skin, thyroid, and testis. This is the first report on the complete sequence of cDNA nucleotides and deduced amino acids of POMC in reptile.

Amino Acid Sequence↗
PubMed1998

N-methyl-D-aspartate-mediated bulbospinal respiratory drive is pH/P(CO2)-insensitive in turtle brainstem-spinal cord.

A split-bath in vitro brainstem-spinal cord preparation from adult turtles (Pseudemys scripta) was used to test the hypotheses that: (1) bulbospinal respiratory synaptic transmission is mediated, at least in part, by N-methyl-D-aspartate (NMDA) glutamatergic receptors, and (2) this transmission is suppressed by low spinal pH (induced by hypercapnea). Recordings from intact pectoralis (expiratory) and serratus (inspiratory) nerves showed that the in vitro turtle brainstem-spinal cord preparation produces phasic expiratory and inspiratory bursts of activity similar to that produced by intact turtles. Bath application of AP-5 [(+/-)-2-amino-5-phosphonopentanoic acid, a noncompetitive NMDA receptor antagonist] to the spinal cord reversibly reduced pectoralis and serratus burst amplitude. In contrast, lowering the pH from 8.04 to 6.94 did not alter burst amplitude in either pectoralis or serratus nerves. These data suggest that spinal NMDA receptors: (1) mediate part of the bulbospinal respiratory synaptic transmission, and (2) are pH/P(CO2)-insensitive. The pH/P(CO2)-insensitivity of NMDA-dependent bulbospinal respiratory synaptic transmission may represent an important adaptation in turtles.

Animals↗
PubMed1997

Open loop optokinetic responses of the turtle.

Turtle eye movements were measured during full-field horizontal optokinetic stimulation under closed and open loop conditions. Because these animals display unyoked slow-phase eye movement behavior, open loop stimulation could not be presented to a paralyzed eye, while monitoring the position of the contralateral eye. The turtle's optokinetic reflex loop was opened electronically by a continuous adjustment of the pattern's position that effectively canceled the effect of the movement of the recorded eye. The highest open loop gains (2-3) were observed at low speeds (< 1 deg/sec), demonstrating a more limited speed range and lower gain in turtle than in the mammalian optokinetic system. These results in the intact animal can be correlated with the visual response properties of the turtle's pretectum and accessory optic system recorded in vitro.

Animals↗
PubMed2001

Induction of the respiratory burst in turtle peritoneal macrophages by Salmonella muenchen.

Peritoneal macrophages were collected from juvenile turtles 72h after intraperitoneal inoculation with a 3% Sephadex suspension. The macrophages were assayed for their chemiluminescent (CL) properties, reflecting their respiratory burst activity, after stimulation with Zymosan A, phorbol 12-myristate 13-acetate (PMA), N-formyl-methionyl-leucyl-phenylalanine (fMLP), and calcium ionophore A23187. Except for fMLP, all triggering agents induced a marked CL response. Luminol was used as the chemiluminescent probe. When comparing CL responses in temperatures ranging from 15 to 35 degrees C, lower assay temperatures induced lower and slower CL responses. Stimulation with viable Salmonella muenchen resulted in a distinct response. Bacteria, inactivated by means of heat or acetone, induced a faster and stronger oxidative burst. Opsonization of either viable or heat-inactivated S. muenchen with non-inactivated anti-S. muenchen serum, prepared in turtles, induced faster and higher CL responses. On the other hand, opsonization of acetone-inactivated S. muenchen caused CL responses to be slower and weaker. S. muenchen, opsonized with heat-inactivated turtle anti S. muenchen serum, induced higher responses than non-opsonized bacteria, but slower and weaker responses than bacteria opsonized with native turtle antiserum. No response was recorded after stimulation with LPS and the supernatant of heat-inactivated bacteria.

Acetone↗
PubMed2003

Spatial reversal learning deficit after medial cortex lesion in turtles.

Many comparative pieces of research support the hypothesis that the medial cortex region of the reptilian forebrain could be homologous to hippocampal formation. Besides, there is some evidence involving this structure in complex spatial learning in a similar manner to hippocampus of mammals and birds. In this experiment we examined effects of medial cortex lesion in reversal learning. Turtles were trained in a spatial and a non-spatial maze procedure and the reversal of these tasks. Data revealed that sham and medial cortex lesioned turtles of both procedures performed well on the initial learning (acquisition). However, during the reversal phase, only the turtles with medial cortex lesion showed impaired performance in the spatial procedure. These results suggest that turtles possess different spatial learning and memory systems in close parallel to those described in other vertebrates, and that medial cortex plays a crucial role in complex place learning.

Animals↗
PubMed1997

Brain Na+/K+-ATPase activity in two anoxia tolerant vertebrates: crucian carp and freshwater turtle.

The crucian carp (Carassius carassius) and freshwater turtles (Trachemys scripta) are among the very few vertebrates that can survive extended periods of anoxia. The major problem for an anoxic brain is energy deficiency. In the brain, the Na+/K+-ATPase is the single most ATP consuming enzyme, being responsible for maintaining ion gradients. We here show that the Na+/K+-ATPase activity in the turtle brain is reduced by 31% in telencephalon and by 34% in cerebellum after 24 h of anoxia. Both changes were reversed upon reoxygenation. By contrast, the Na+/K+-ATPase activities were maintained in the anoxic crucian carp brain. These results support the notion that crucian carp and turtles use divergent strategies for anoxic survival. The fall in Na+/K+-ATPase activities displayed by the turtle is likely to be related to the strong depression of brain electric and metabolic activity utilized as an anoxic survival strategy by this species.

Animals↗
PubMed1997

Purification and partial amino acid sequences of two distinct albumins from turtle plasma.

Two putative albumins, denoted Alb-1 (apparent molecular mass of 67 kDa) and Alb-2 (68 kDa), were purified from plasma of the emydid turtle (Trachemys scripta). Concentrations in serum or plasma were determined by radioimmunoassay using 125I-labeled Alb-1. In juvenile turtles (less than 2 years of age), serum concentrations of Alb-1 and Alb-2 were 2.72 +/- 0.23 mg/ml and 1.68 +/- 0.22 mg/ml, respectively, while concentrations in plasma pooled from adult turtles were 4.2 mg/ml and 2.6 mg/ml, respectively. The two albumins are immunologically distinct from one another as determined by both radioimmunoassay with 125I-labeled Alb-1 and Western blot analysis with antichicken albumin antiserum. Determination of the amino acid compositions of Alb-1 and Alb-2, and of albumin purified from plasma of the common snapping turtle (Chelydra serpentina), suggested that Alb-1 is more similar to albumins of other animals than is Alb-2. This was also indicated by Western blot analysis and by determining the N-terminal amino acid sequences of Alb-1 (40 residues) and Alb-2 (15 residues). Thus, it appears that two distinct forms of albumin are synthesized by T. scripta, possibly as a result of gene duplication and divergence.

Amino Acid Sequence↗
PubMed2000

Effects of acute fresh water exposure on water flux rates and osmotic responses in Kemp's ridley sea turtles (Lepidochelys kempi).

Water flux rates and osmotic responses of Kemp's Ridley sea turtles (Lepidochelys kempi) acutely exposed to fresh water were quantified. Salt-water adapted turtles were exposed to fresh water for 4 d before being returned to salt water. During the initial salt water phase, absolute and relative water flux rates were 1.2+/-0.1 l d(-1) and 123.0+/-6.8 ml kg(-1) d(-1), respectively. When turtles were exposed to fresh water, rates increased by approximately 30%. Upon return to salt water, rates decreased to original levels. Plasma osmolality, Na(+), K(+), and Cl(-) decreased during exposure to fresh water, and subsequently increased during the return to salt water. The Na(+):K(+) ratio was elevated during the fresh water phase and subsequently decreased upon return to salt water. Aldosterone and corticosterone were not altered during exposure to fresh water. Elevated water flux rates during fresh water exposure reflected an increase in water consumption, resulting in a decrease in ionic and osmotic concentrations. The lack of a change in adrenocorticoids to acute fresh water exposure suggests that adrenal responsiveness to an hypo-osmotic environment may be delayed in marine turtles when compared to marine mammals.

Adaptation, Physiological↗
PubMed2003

Gap junctions do not underlie changes in whole-cell conductance in anoxic turtle brain.

An acute reduction in cell membrane permeability could provide an effective strategy to prolong anoxic survival. A previous study has shown that in the western painted turtle whole-cell neuronal conductance (G(w)) decreases during anoxia, which may be mediated by the activation of adenosine A(1) receptors and calcium. Reduction in G(w) is thought to be the result of ion channel closure, but closure of gap junctions could also be responsible for this phenomenon. In our study, antibody staining of connexin 32 and 43 (Cx32 and Cx43) suggested the presence of gap junctional components in the turtle cortex. To examine if gap junctions were involved in the previously measured anoxic decrease in G(w), neuronal connectivity was assessed through the measurement of whole-cell capacitance (C(w)). Turtle cortical sheets were perfused with normoxic (95%O(2)/5%CO(2)), anoxic (95%N(2)/5%CO(2)), high calcium (4 mM) and adenosine (200 microm) artificial cerebral spinal fluid (aCSF). No significant change in C(w) was observed under any of the above conditions. However, during hypo-osmotic aCSF perfusion C(w) decreased significantly, with the lowest value of 50+/-10.4 pF (P<0.05) occurring at 30 min. To visualize changes in gap junction permeability lucifer yellow was loaded into turtle neurons during normoxic, anoxic, 0 calcium, hypo-osmotic, cold shock, (+)-isoproterenol, nitric oxide donor S-nitoso-acetyl penicillamine, and 8-bromo-guanosine 3',5'-cyclic monophosphate aCSF perfusion. Dye propagation was only observed in 3 of 20 cold shock experiments (4 degrees C). We conclude that gap junctions are not involved in the acute reduction in G(w) previously observed during anoxia and that our results support the hypothesis that ion channel arrest is involved.

Animals↗
PubMed2003

Natural freeze-tolerance in hatchling painted turtles?

Hatchlings of the North American painted turtle (Family Emydidae: Chrysemys picta) typically spend their first winter of life inside a shallow, subterranean hibernaculum (the natal nest) where life-threatening conditions of ice and cold commonly occur. Although a popular opinion holds that neonates exploit a tolerance for freezing to survive the rigors of winter, hatchlings are more likely to withstand exposure to ice and cold by avoiding freezing altogether-and to do so without the benefit of an antifreeze. In the interval between hatching by turtles in late summer and the onset of wintery weather in November or December, the integument of the animals becomes highly resistant to the penetration of ice into body compartments from surrounding soil, and the turtles also purge their bodies of catalysts for the formation of ice. These two adjustments, taken together, enable the animals to supercool to temperatures below those that they routinely experience in nature. However, cardiac function in hatchlings is diminished at subzero temperatures, thereby compromising the delivery of oxygen to peripheral tissues and eliciting an increase in reliance by those tissues on anaerobic metabolism for the provision of ATP. The resulting increase in production of lactic acid may disrupt acid/base balance and lead to death even in animals that remain unfrozen. Although an ability to undergo supercooling may be key to survival by overwintering turtles in northerly populations, a similar capacity to resist inoculation and undergo supercooling characterizes animals from a population near the southern limit of distribution, where winters are relatively benign. Thus, the suite of characters enabling hatchlings to withstand exposure to ice and cold may have been acquired prior to the northward dispersal of the species at the end of the Pleistocene, and the characters may not have originated as adaptations specifically to the challenges of winter.

Acclimatization↗