Adaptations to neoteny in the salamander, Necturus maculosus. Blood respiratory properties and interactive effects of pH, temperature and ATP on hemoglobin oxygenation

Weber, Roy E.; Wells, R. M. G.; Rossetti, J. E.

doi:10.1016/0300-9629(85)90403-7

Cited by 21 publications

(7 citation statements)

References 36 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…The association of deoxygenated tetramers provides an explanation for the unusually high Hill coefficients obtained for the blood of R. catesbeiana and other frogs (49,63,130), for the blood of all birds examined and that of some lizards, turtles, and snakes (48,64,101,131), but not salamanders (129). The birds whose blood showed high Hill coefficients include the rhea, mallard, pigeon, chicken, quail, sparrow, and hummingbird (47, 59, 61, 62).…”

Section: Association Of Tetramersmentioning

confidence: 87%

The Bohr Effect

Riggs¹

1988

Annu. Rev. Physiol.

173

View full text Add to dashboard Cite

Whatever you do in one part of the molecule affects the molecule as a whole." M. F. Perutz (9 1) INTRODUCTIONThe control of oxygen binding by hemoglobin (Hb) with pH is of profound importance in facilitating gas exchange in blood. This modulation, known as the Bohr effect, reflects the fact that protons are released upon Hb oxygena tion at physiological pH (the alkaline Bohr effect), and protons are taken up upon oxygenation at low pH (the acid or reversed Bohr effect). Reciprocally, changes in pH modulate oxygen affinity. These proton exchanges arise because conformational changes in the Hb associated with ligand binding at the heme result in pK changes in certain acid groups that are distant from the heme. Changes in proton binding also result from differential interaction of buffer ions with oxy-and deoxy-Hb (3,18). The binding of salt ions can be considered a special kind of Bohr effect (3). Resonance Raman spectroscopy shows that the iron-proximal histidine stretching motion is exquisitely sensi tive to amino acid substitutions distant from the heme (34). This review examines recent experiments to determine which groups are responsible for the Bohr effect and how these ligand-linked processes are modulated by other allosteric factors, e.g. buffer ions, organic phosphates, CO2, and chloride, all of which lower the oxygen affinity of Hb by preferential binding to deoxy-Hb. A central problem has been to determine the relative quantitative roles of different ionizable groups responsible for in the Bohr effect. What kinds and numbers of groups are involved? Attempts have been made to calculate pK values by using electrostatic theory. How do such electrostatic calculations compare with other methods for estimating the contributions of different groups? 181 0066-4278/88/0315-0181$02.00Annu. Rev. Physiol. 1988.50:181-204. Downloaded from www.annualreviews.org by North Dakota INBRE on 09/15/13. For personal use only. Quick links to online content Further ANNUAL REVIEWS 182 RIGGS Perutz (89) proposed a stereochemical model that provided a molecular explanation of both the Bohr effect and of cooperativity of oxygen binding. The model rested initially on differences between the x-ray structures de termined for horse deoxy-and oxy-like metHb. The model has been modified and refined as a result of many subsequent experiments and higher resolution x-ray analyses on human deoxy-Hb, HbCO, and Hb02 (8, 33,96,112). Although the original proposal depended on the structure of metHb, which was found to be isomorphous with Hb02, some differences between the met, CO, and oxy derivatives do exist (33,112). This is shown most simply by the pronounced differences in solubility: human HbCO is over 40% more soluble than Hb02 in phosphate buffers at 10°C and 67% more soluble than metHb; deoxy-Hb is only one tenth as soluble as HbCO (50). The differences in surface topology responsible for these solubility effects are unknown. How ever, the distal histidine of the a subunit is much closer to the heme axis in Hb02 than in HbCO (112). Presu...

show abstract

Section: Association Of Tetramersmentioning

confidence: 87%

The Bohr Effect

Riggs¹

1988

Annu. Rev. Physiol.

173

View full text Add to dashboard Cite

show abstract

“…The heat of oxygenation-linked reactions with allosteric effectors was assessed as the difference between HЈ values in the presence and absence of these ligands (cf. Weber et al, 1985;Weber et al, 2008).…”

Section: Methodsmentioning

confidence: 99%

ATP-induced temperature independence of hemoglobin–O2 affinity in heterothermic billfish

Weber

Campbell

Fago

et al. 2010

Journal of Experimental Biology

View full text Add to dashboard Cite

SUMMARYThe inverse relationship between temperature and hemoglobin-O 2 affinity resulting from the exothermic nature of heme oxygenation favors O 2 unloading from blood to warm, metabolically active tissues. However, this temperature sensitivity is maladaptive, and commonly countered in regional heterotherms, where it may hamper unloading (e.g. in cold extremities of arctic mammals) or increase the diffusive arterio-venous short-circuiting of O 2 (e.g. in counter-current heat exchangers of warm swimming muscles of tuna). We hypothesized analogous blood specializations in heterothermic billfish, whose warm eyes and brains increase the temporal resolution of vision, and measured hemoglobin-O 2 binding properties in three species over a wide pH range, at two temperatures, and in the absence and presence of the major red cell effector, ATP, permitting detailed assessment of overall oxygenation enthalpies (⌬HЈ) and contributions from oxygenation-linked proton and ATP dissociation. . Thus in addition to allosterically modulating hemoglobin-O 2 affinity, ATP diminishes its temperature sensitivity, reducing deleterious arterio-venous short-circuiting of oxygen in the cranial billfish heat exchangers. The mechanism underlying this reduction in oxygenation enthalpy differs fundamentally from that in tuna, supporting independent evolution of this trait in these scombroid lineages.

show abstract

“… References: 1 Moalli et al (1981); 2 Boutilier & Toews (1981 b ); 3 Jerret & Mays (1973); 4 Solis et al (2007); 5 Lenfant & Johansen (1967); 6 Weber et al (1985); 7 Gahlenbeck & Bartels (1970); 8 Heisler et al (1982); 9 Toews et al (1971) (highly variable both within and between individuals). …”

Section: Species Accountsmentioning

confidence: 99%

Metabolism, gas exchange, and acid‐base balance of giant salamanders

Ultsch

2011

Biological Reviews

View full text Add to dashboard Cite

The giant salamanders are aquatic and paedomorphic urodeles including the genera Andrias and Cryptobranchus (Cryptobranchidae), Amphiuma (Amphiumidae), Siren (Sirenidae), and Necturus (Proteidae, of which only N. maculosus is considered 'a giant'). Species in the genera Cryptobranchus and Necturus are considered aquatic salamanders well adapted for breathing water, poorly adapted for breathing air, and with limited abilities to compensate acid-base disturbances. As such, they are water-breathing animals with a somewhat fish-like respiratory and acid-base physiology, whose habitat selection is limited to waters that do not typically become hypoxic or hypercarbic (although this assertion has been questioned for N. maculosus). Siren and Amphiuma species, by contrast, are dependent upon air-breathing, have excellent lungs, inefficient (Siren) or no (Amphiuma) gills, and are obligate air-breathers with an acid-base status more similar to that of terrestrial tetrapods. As such, they can be considered to be air-breathing animals that live in water. Their response to the aquatic hypercarbia that they often encounter is to maintain intracellular pH (pH(i) ) and abandon extracellular pH regulation, a process that has been referred to as preferential pH(i) regulation. The acid-base status of some present-day tropical air-breathing fishes, and of Siren and Amphiuma, suggests that the acid-base transition from a low PCO(2) -low [] system typical of water-breathing fishes to the high PCO(2) -high [] systems of terrestrial tetrapods may have been completed before emergence onto land, and likely occurred in habitats that were typically both hypoxic and hypercarbic.

show abstract

Adaptations to neoteny in the salamander, Necturus maculosus. Blood respiratory properties and interactive effects of pH, temperature and ATP on hemoglobin oxygenation

Cited by 21 publications

References 36 publications

The Bohr Effect

The Bohr Effect

ATP-induced temperature independence of hemoglobin–O2 affinity in heterothermic billfish

Metabolism, gas exchange, and acid‐base balance of giant salamanders

Contact Info

Product

Resources

About