Structural basis of Na+/K+-ATPase adaptation to marine environments

Colina, Claudia; Rosenthal, Joshua J. C.; DeGiorgis, Joseph A.; Srikumar, Deepa; Iruku, Nikhila; Holmgren, Miguel

doi:10.1038/nsmb1237

Cited by 32 publications

(39 citation statements)

References 42 publications

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“…Na + /K + -ATPase orthologs isolated from multiple cold-and warm-adapted species exhibited a similar segregation of thermal sensitivities. (Colina et al, 2007)]. To obtain a consensus sequence, multiple cDNA clones were sequenced to completion.…”

Section: Introductionmentioning

confidence: 99%

Physiological adaptation of an Antarctic Na+/K+-ATPase to the cold

Galarza-Muñoz

Soto-Morales

Holmgren

et al. 2011

Journal of Experimental Biology

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SUMMARYBecause enzymatic activity is strongly suppressed by the cold, polar poikilotherms face significant adaptive challenges. For example, at 0°C the catalytic activity of a typical enzyme from a temperate organism is reduced by more than 90%. Enzymes embedded in the plasma membrane, such as the Na + /K + -ATPase, may be even more susceptible to the cold because of thermal effects on the lipid bilayer. Accordingly, adaptive changes in response to the cold may include adjustments to the enzyme or the surrounding lipid environment, or synergistic changes to both. To assess the contribution of the enzyme itself, we cloned orthologous Na + /K + -ATPase -subunits from an Antarctic (Pareledone sp.; -1.8°C) and a temperate octopus (Octopus bimaculatus; ~18°C), and compared their turnover rates and temperature sensitivities in a heterologous expression system. The primary sequences of the two pumps were found to be highly similar (97% identity), with most differences being conservative changes involving hydrophobic residues. The physiology of the pumps was studied using an electrophysiological approach in intact Xenopus oocytes. The voltage dependence of the pumps was equivalent. However, at room temperature the maximum turnover rate of the Antarctic pump was found to be 25% higher than that of the temperate pump. In addition, the Antarctic pump exhibited a lower temperature sensitivity, leading to significantly higher relative activity at lower temperatures. Orthologous Na + /K + pumps were then isolated from two tropical and two Arctic octopus. The temperature sensitivities of these pumps closely matched those of the temperate and Antarctic pumps, respectively. Thus, reduced thermal sensitivity appears to be a common mechanism driving cold adaptation in the Na + /K + -ATPase. Supplementary material available online at

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Section: Introductionmentioning

confidence: 99%

Physiological adaptation of an Antarctic Na+/K+-ATPase to the cold

Galarza-Muñoz

Soto-Morales

Holmgren

et al. 2011

Journal of Experimental Biology

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“…Two consequences of the unequal transport stoichiometry of Na þ and K þ are that steady pumping produces an outwardly directed current (1), proportional in magnitude to the turnover rate (2), which can be monitored electrically (3)(4)(5)(6)(7)(8), and that at least one step in the transport cycle must move charge through the membrane field (9). The latter implies that, under favorable conditions, charge relaxations following voltage jumps can be used to learn details about specific steps during the transport cycle (10)(11)(12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28).…”

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confidence: 99%

Energy landscape of the reactions governing the Na ⁺ deeply occluded state of the Na ⁺ /K ⁺ -ATPase in the giant axon of the Humboldt squid

Castillo

Giorgis

Basilio

et al. 2011

Proc. Natl. Acad. Sci. U.S.A.

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The Na ∕K pump is a nearly ubiquitous membrane protein in animal cells that uses the free energy of ATP hydrolysis to alternatively export 3Na from the cell and import 2K per cycle. This exchange of ions produces a steady-state outwardly directed current, which is proportional in magnitude to the turnover rate. Under certain ionic conditions, a sudden voltage jump generates temporally distinct transient currents mediated by the Na ∕K pump that represent the kinetics of extracellular Na binding/release and Na occlusion/deocclusion transitions. For many years, these events have escaped a proper thermodynamic treatment due to the relatively small electrical signal. Here, taking the advantages offered by the large diameter of the axons from the squid Dosidicus gigas, we have been able to separate the kinetic components of the transient currents in an extended temperature range and thus characterize the energetic landscape of the pump cycle and those transitions associated with the extracellular release of the first Na from the deeply occluded state. Occlusion/deocclusion transition involves large changes in enthalpy and entropy as the ion is exposed to the external milieu for release. Binding/unbinding is substantially less costly, yet larger than predicted for the energetic cost of an ion diffusing through a permeation pathway, which suggests that ion binding/unbinding must involve amino acid sidechain rearrangements at the site.P-type ATPases | pump currents | thermodynamics D uring each normal transport cycle of the Na þ ∕K þ -ATPase pump, three Na þ are exported from the cell in exchange for two K þ imported, a process driven by hydrolysis of one molecule of ATP. By establishing the Na þ and K þ gradients across cell membranes, the Na þ ∕K þ pump enables action potentials, synaptic signaling, and most solute transport in and out of cells. Two consequences of the unequal transport stoichiometry of Na þ and K þ are that steady pumping produces an outwardly directed current (1), proportional in magnitude to the turnover rate (2), which can be monitored electrically (3)(4)(5)(6)(7)(8), and that at least one step in the transport cycle must move charge through the membrane field (9). The latter implies that, under favorable conditions, charge relaxations following voltage jumps can be used to learn details about specific steps during the transport cycle (10-28).In the absence of internal and external K þ , the nominal absence of internal ADP and presence of an ATP regenerating system, the Na þ ∕K þ pump allows exchange of 3Na þ between their binding sites in a deeply occluded conformation and the external milieu (21, 29) ( Fig. 1A; encircled by dotted lines). Under these conditions there is no steady pump current observed at any voltage. Nevertheless, sudden voltage steps produce pre-steadystate currents that can be recorded (12, 13, 16-18, 21, 23, 26).These currents allow direct measurements of the rates of partial reactions of the pump cycle. Using giant axons from the squid Loligo pealeii, we have characterized th...

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“…The Na + / K + -ATPase in marine environment was reported to have more positive amino acids in extracellular Na + exit pathway, to reduce its sensitivity to external Na + ions 16) . Gly319 on TM3-4 loop in Loligo Na + /K + -ATPase, conserved among the Na pumps of marine animals and one of the important residues for the high Na + adaptation.…”

Section: Discussionmentioning

confidence: 99%

Homology Modeling of an Algal Membrane Protein, Heterosigma Akashiwo Na+–ATPase

Shono

Wada

et al. 2010

membrane

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Original Contribution： MEMBRANE， 35（2），80 85（2010）The three-dimensional structure of Heterosigma akashiwo Na + -ATPase (HANA) was predicted by means of homology modeling based on the crystal structure of the K + -bound form of shark Na + /K + -ATPase (PDB ID: 2ZXE). The overall structure of HANA appears to be similar to that of shark Na + /K + -ATPase. Both contain three characteristic cytoplasmic domains, A, N and P, which are unique to P-type ATPases. HANA has a long TM7-8 junction as a large extracellular domain, in place of the β-subunit of shark Na + /K + -ATPase. Two putative K + -binding sites in the transmembrane domain of HANA were identified by means of valence mapping based on the constructed structure. The presence of K + -binding sites and the reported ion requirements for ATPase activity and EP formation indicate that HANA may transport K + ions in the same manner as animal Na + /K + -ATPases.

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Structural basis of Na+/K+-ATPase adaptation to marine environments

Cited by 32 publications

References 42 publications

Physiological adaptation of an Antarctic Na+/K+-ATPase to the cold

Physiological adaptation of an Antarctic Na+/K+-ATPase to the cold

Energy landscape of the reactions governing the Na ⁺ deeply occluded state of the Na ⁺ /K ⁺ -ATPase in the giant axon of the Humboldt squid

Homology Modeling of an Algal Membrane Protein, Heterosigma Akashiwo Na+–ATPase

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Structural basis of Na+/K+-ATPase adaptation to marine environments

Cited by 32 publications

References 42 publications

Physiological adaptation of an Antarctic Na+/K+-ATPase to the cold

Physiological adaptation of an Antarctic Na+/K+-ATPase to the cold

Energy landscape of the reactions governing the Na + deeply occluded state of the Na + /K + -ATPase in the giant axon of the Humboldt squid

Homology Modeling of an Algal Membrane Protein, Heterosigma Akashiwo Na+–ATPase

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Energy landscape of the reactions governing the Na ⁺ deeply occluded state of the Na ⁺ /K ⁺ -ATPase in the giant axon of the Humboldt squid