Two Ca2+ ATPase genes: Homologies and mechanistic implications of deduced amino acid sequences

doi:10.1016/0092-8674(86)90269-2

Cell

Volume 44, Issue 4, 28 February 1986, Pages 597-607

https://doi.org/10.1016/0092-8674(86)90269-2 Get rights and content

Abstract

Rabbit genomic DNA contains two genes that encode Ca²⁺ ATPases of fast twitch and of slow twitch (and cardiac) sarcoplasmic reticulum, respectively. The deduced amino acid sequences of the products of the two genes are highly conserved in putative Ca²⁺ binding regions, in sectors leading from cytoplasmic domains into transmembrane domains, and in transmembrane helices. A transport mechanism is proposed in which Ca²⁺ binds to negatively charged groups on amphipathic stalk sectors, becoming occluded during enzyme phosphorylation by bound ATP. Rotation of the stalk sectors is induced as the energy in the phosphorylated enzyme (E₁P) is utilized in conformational changes leading to the low energy form, E₂P. Rotation leads to disruption of high affinity Ca²⁺ binding sites and release of Ca²⁺ into a charge-lined membrane channel. Ca²⁺ then traverses the membrane by exchange diffusion.

References (72)

G. Allen et al.
A 31 residue tryptic peptide from the active site of the Ca²⁺-transporting adenosine triphosphatase of rabbit sarcoplasmic reticulum
FEBS Lett.
(1976)
J.K. Blasie et al.
Time resolved X-ray diffraction studies of the sarcoplasmic reticulum membrane during active transport
Biophys. J.
(1985)
L. Dux et al.
Crystallization of the Ca²⁺ ATPase of sarcoplasmic reticulum by calcium and lanthanide ions
J. Biol. Chem.
(1985)
F. Fernandez-Belda et al.
A comparative study of calcium transients by isotopic tracer, metallochromic indicator, and intrinsic fluorescence in sarcoplasmic reticulum ATPase
J. Biol. Chem.
(1984)
J.E. Hall et al.
Alamethicin
A rich model for channel behaviour
Biophys. J.
(1984)
S.R. Highsmith et al.
Nd³⁺ and Co²⁺ binding to sarcoplasmic reticulum CaATPase
An estimation of the distance from the ATP binding site to the high-affinity calcium binding sites
J. Biol. Chem.
(1984)
S.B. Hladky et al.
Ion movements in gramicidin channels
Curr. Top. Membr. Transp.
(1984)
L. Hymel et al.
Target size of calcium pump protein from skeletal muscle sarcoplasmic reticulum
J. Biol. Chem.
(1984)
A. Klip et al.
Alignment of the major tryptic fragments of the adenosine triphosphatase from sarcoplasmic reticulum
J. Biol. Chem.
(1980)
D.H. MacLennan et al.
Biosynthesis of sarcoplasmic reticulum proteins
Meth. Enzymol.
(1983)

T.J. McIntosh et al.

Alamethicin-induced changes in lipid bilayer morphology

Biochim. Biophys. Acta

(1982)

J. Messing

New M13 vectors for cloning

Meth. Enzymol.

(1983)

C. Mitchinson et al.

Identification of a labelled peptide after stoicheiometric reaction of fluorescein isothiocyanate with the Ca²⁺-dependent adenosine triphosphatase of sarcoplasmic reticulum

FEBS Lett.

(1982)

E. Nickel et al.

Ultrastucture of isolated membrane of Torpedo electric tissue

Brain Res.

(1973)

R.A.F. Reithmeier et al.

Assembly of the sarcoplasmic reticulum

Cell free synthesis of the Ca²⁺ + Mg²⁺-adenosine triphosphatase and calsequestrin

J. Biol. Chem.

(1980)

J.S. Richardson

The anatomy and taxonomy of protein structure

Adv. Protein Struct.

(1981)

A. Schwartz et al.

The rate of calcium uptake into sarcoplasmic reticulum of cardiac muscle and skeletal muscle

Effects of cyclic AMP-dependent protein kinase and phosphorylase b kinase

Biochim. Biophys. Acta.

(1976)

T.L. Scott

Distances between the functional sites of the Ca²⁺ + Mg²⁺ ATPase of sarcoplasmic reticulum

J. Biol. Chem.

(1985)

V. Sgaramella et al.

Total synthesis of the structural gene for an alanine transfer RNA from yeast

Enzymic joining of the chemically synthesized polydeoxy-nucleotides to form the DNA duplex representing nucleotide sequence 1 to 20

J. Mol. Biol.

(1972)

E.M. Southern

Detection of specific sequences among DNA fragments separated by gel electrophoresis

J. Mol. Biol.

(1975)

P.S. Stewart et al.

Surface particles of sarcoplasmic reticulum membranes

Structural features of the adenosine triphosphatase

J. Biol. Chem.

(1974)

H. Takisawa et al.

Occlusion of calcium in the ADP-sensitive phosphoenzyme of the adenosine triphosphatase of sarcoplasmic reticulum

J. Biol. Chem.

(1983)

C. Tanford

The sarcoplasmic reticulum calcium pump

Localization of free energy transfer to discrete steps of the reaction cycle

FEBS Lett.

(1984)

C.H. Tate et al.

Nucleotide specificity of cardiac sarcoplasmic reticulum

GTP-induced calcium accumulation and GTPase activity

J. Biol. Chem.

(1985)

W.R. Taylor et al.

Recognition of supersecondary structure in proteins

J. Mol. Biol.

(1984)

K. Taylor et al.

Structure of the vanadate-induced crystals of sarcoplasmic reticulum Ca²⁺-ATPase

J. Mol. Biol.

J.P. Andersen et al.

Direct demonstration of structural changes in soluble, monomeric Ca²⁺ ATPase associated with Ca²⁺ release during the transport cycle

H.C. Birnboim et al.

A rapid alkaline extraction procedure for screening recombinant plasmid DNA

Nucl. Acids Res.

(1979)

I.A. Brody

Muscle contraction induced by exercise

A syndrome attributable to decreased relaxing factor

N. Eng. J. Med.

(1969)

L. de Meis et al.

Energy interconversion by the Ca²⁺-dependent ATPase of the sarcoplasmic reticulum

Ann. Rev. Biochem.

(1979)

L. Dente et al.

pEMBL: a new family of single stranded plasmids

Nucl. Acids Res.

(1983)

Cited by (668)

ERMA (TMEM94) is a P-type ATPase transporter for Mg<sup>2+</sup> uptake in the endoplasmic reticulum
2024, Molecular Cell
Intracellular Mg²⁺ (_iMg²⁺) is bound with phosphometabolites, nucleic acids, and proteins in eukaryotes. Little is known about the intracellular compartmentalization and molecular details of Mg²⁺ transport into/from cellular organelles such as the endoplasmic reticulum (ER). We found that the ER is a major _iMg²⁺ compartment refilled by a largely uncharacterized ER-localized protein, TMEM94. Conventional and AlphaFold2 predictions suggest that ERMA (TMEM94) is a multi-pass transmembrane protein with large cytosolic headpiece actuator, nucleotide, and phosphorylation domains, analogous to P-type ATPases. However, ERMA uniquely combines a P-type ATPase domain and a GMN motif for _ERMg²⁺ uptake. Experiments reveal that a tyrosine residue is crucial for Mg²⁺ binding and activity in a mechanism conserved in both prokaryotic (mgtB and mgtA) and eukaryotic Mg²⁺ ATPases. Cardiac dysfunction by haploinsufficiency, abnormal Ca²⁺ cycling in mouse Erma^+/− cardiomyocytes, and ERMA mRNA silencing in human iPSC-cardiomyocytes collectively define ERMA as an essential component of _ERMg²⁺ uptake in eukaryotes.
Metagenomic assembled genomes unravel purple non‑sulfur bacteria (PNSB) involved in integrating C, N, P biotransformation
2022, Science of the Total Environment
Purple non‑sulfur bacteria (PNSB) based bioprocess has been developed to remove carbon, nitrogen and phosphorus from wastewater. However, the interactions of various bioconversion of carbon (C), nitrogen (N) and phosphorus (P) are not completely clear. In this study, a genome-centric metagenomic approach was employed to delineate the shift in microbial community structures and functional genes under light and dark conditions. Seven and 22 metagenomic assembled genomes (MAGs) were recovered from samples in light and dark conditions, accounting for a substantial portion of microbes. Under light, Rhodopseudomonas palustris promoted complex metabolic processes and interactions for C, N and P conversions. Burkholderia contaminans was discovered as new potential organisms for simultaneous C, N and P removal. Metagenomics analysis confirmed genes involved in the synthesis of glycogen, poly-β-hydroxybutyrate, poly-P, amino acids and carotenoids in R. palustris. The substrate transformation mechanisms and potential pathways were proposed according to the detected metabolites. Our findings provided insights into a new biological system with simultaneous C, N and P bioconversions, and improved the understanding of interactions among the key populations.
Calcium signaling and regulation of ecdysteroidogenesis in crustacean Y-organs
2021, General and Comparative Endocrinology
Crustacean Y-organs secrete ecdysteroid molting hormones. Ecdysteroids are released in increased amount during premolt, circulate in hemolymph, and stimulate the events in target cells that lead to molting. During much of the molting cycle, ecdysteroid production is suppressed by molt-inhibiting hormone (MIH), a peptide neurohormone produced in the eyestalks. The suppressive effect of MIH is mediated by a cyclic nucleotide second messenger. A decrease in circulating MIH is associated with an increase in the hemolymphatic ecdysteroid titer during pre-molt. Nevertheless, it has long been hypothesized that a positive regulatory signal or stimulus is also involved in promoting ecdysteroidogenensis during premolt. Data reviewed here are consistent with the hypothesis that an intracellular Ca²⁺ signal provides that stimulus. Pharmacological agents that increase intracellular Ca²⁺ in Y-organs promote ecdysteroidogenesis, while agents that lower intracellular Ca²⁺ or disrupt Ca²⁺ signaling suppress ecdysteroidogenesis. Further, an increase in the hemolymphatic ecdysteroid titer after eyestalk ablation or during natural premolt is associated with an increase in intracellular free Ca²⁺ in Y-organ cells. Several lines of evidence suggest elevated intracellular calcium is linked to enhanced ecdysteroidogenesis through activation of Ca²⁺/calmodulin dependent cyclic nucleotide phosphodiesterase, thereby lowering intracellular cyclic nucleotide second messenger levels and promoting ecdysteroidogenesis. Results of transcriptomic studies show genes involved in Ca²⁺ signaling are well represented in Y-organs. Several recent studies have focused on Ca²⁺ transport proteins in Y-organs. Complementary DNAs encoding a plasma membrane Ca²⁺ ATPase (PMCA) and a sarcoplasmic/endoplasmic reticulum Ca²⁺ ATPase (SERCA) have been cloned from crab Y-organs. The relative abundance of PMCA and SERCA transcripts in Y-organs is elevated during premolt, a time when Ca²⁺ levels in Y-organs are likewise elevated. The results are consistent with the notion that these transport proteins act to maintain the Ca²⁺ gradient across the cell membrane and re-set the cell for future Ca²⁺ signals.
Nesfatin-1-like peptide is a negative regulator of cardiovascular functions in zebrafish and goldfish
2021, General and Comparative Endocrinology
Nucleobindins (NUCB1 and NUCB2) were originally identified as calcium and DNA binding proteins. Nesfatin-1 (NEFA/nucleobindin-2-Encoded Satiety and Fat-Influencing proteiN-1) is an 82 amino acid anorexigenic peptide encoded in the N-terminal region of NUCB2. We have shown that nesfatin-1 is a cardiosuppressor in zebrafish. Both NUCB1 and NUCB2 possess a -very highly conserved bioactive core. It was found that a nesfatin-1-like peptide (NLP) encoded in NUCB1 suppresses food intake in fish. In this research, we investigated whether NLP has nesfatin-1-like effects on cardiovascular functions. NUCB1/NLP-like immunoreactivity was found in the atrium and ventricle of the heart and skeletal muscle of zebrafish. Intraperitoneal injection (IP) of either zebrafish NLP or rat NLP suppressed cardiac functions in both zebrafish and goldfish. Irisin and RyR1b mRNA expression was downregulated by NLP in zebrafish cardiac and skeletal muscles. However, cardiac ATP2a2 mRNA expression was elevated after NLP injection. Administration of scrambled NLP did not affect irisin, RyR1b or ATP2a2 mRNA expression in zebrafish. Together, these results implicate NLP as a suppressor of cardiovascular physiology in zebrafish and goldfish.
Interaction of a dirhamnolipid biosurfactant with sarcoplasmic reticulum calcium ATPase (SERCA1a)
2021, Archives of Biochemistry and Biophysics
The interaction of a dirhamnolipid biosurfactant secreted by Pseudomonas aeruginosa with calcium ATPase from sarcoplasmic reticulum (SR) was studied by means of different approaches, such as enzyme activity, fluorescence spectroscopy, Fourier transform infrared spectroscopy (FTIR), differential scanning calorimetry (DSC), and molecular docking simulations. The ATP hydrolysis activity was fully inhibited by incubation with dirhamnolipid (diRL) up to 0.1 mM concentration, corresponding to a surfactant concentration below membrane solubilization threshold. Surfactant-protein interaction induced conformational changes in the protein observed by an increase in the accessibility of tryptophan residues to the aqueous phase and by changes in the secondary structure of the protein as seen by fluorescence and FTIR spectroscopy. As a consequence, the protein become more unstable and denatured at lower temperatures, as seen by enzyme activity and DSC studies. Finally, these results were explained at molecular level throughout molecular docking simulations. It is concluded that there is a specific dirhamnolipid-protein interaction not related to the surface activity of the surfactant but to the particular physicochemical properties of the biosurfactant molecule.
Molecular cloning and characterization of a sarco/endoplasmic reticulum Ca<sup>2+</sup> ATPase (SERCA) from Y-organs of the blue crab (Callinectes sapidus)
2018, Gene
Existing data indicate that a Ca²⁺ signal stimulates ecdysteroid hormone production by crustacean molting glands (Y-organs). Ca²⁺ signaling is dependent on a tightly regulated Ca²⁺ gradient, with intracellular free Ca²⁺ maintained at a low basal level (typically sub-micromolar). This is achieved through the action of proteins intrinsic to the plasma membrane and the membranes of organelles. One such protein, the sarco/endoplasmic reticulum Ca²⁺ ATPase (SERCA), pumps Ca²⁺ from cytosol to the lumen of the endoplasmic reticulum. As a step toward understanding Ca²⁺-mediated regulation of ecdysteroidogenesis, we have begun investigating Ca²⁺ transport proteins in Y-organs. In studies reported here, we used a PCR-based strategy to clone from Y-organs of the blue crab (Callinectes sapidus) a cDNA encoding a putative SERCA protein. The cloned Cas-SERCA cDNA (3806 bp) includes a 3057-bp open reading frame that encodes a 1019-residue protein (Cas-SERCA). The conceptually translated protein has a predicted molecular mass of 111.42 × 10³ and contains all signature domains of an authentic SERCA, including ten transmembrane domains and a phosphorylation site at aspartate 351. A homology model of Cas-SERCA closely resembles models of related SERCA proteins. Phylogenetic analysis shows Cas-SERCA clusters with SERCA proteins from other arthropods. An assessment of tissue distribution indicates the Cas-SERCA transcript is widely distributed across tissues. Studies using quantitative PCR showed Cas-SERCA transcript abundance increased significantly in Y-organs activated by eyestalk ablation, a pattern consistent with the hypothesis that Cas-SERCA functions to maintain Ca²⁺ homeostasis in Y-organs.

View all citing articles on Scopus

View full text

Cell

ArticleTwo Ca2+ ATPase genes: Homologies and mechanistic implications of deduced amino acid sequences

Abstract

FEBS Lett.

Biophys. J.

J. Biol. Chem.

J. Biol. Chem.

Biophys. J.

J. Biol. Chem.

Curr. Top. Membr. Transp.

J. Biol. Chem.

J. Biol. Chem.

Meth. Enzymol.

Biochim. Biophys. Acta

Meth. Enzymol.

FEBS Lett.

Brain Res.

J. Biol. Chem.

Adv. Protein Struct.

Biochim. Biophys. Acta.

J. Biol. Chem.

J. Mol. Biol.

J. Mol. Biol.

J. Biol. Chem.

J. Biol. Chem.

FEBS Lett.

J. Biol. Chem.

J. Mol. Biol.

J. Mol. Biol.

Cell

The primary structure of the calcium-transporting adenosine triphosphatase of rabbit skeletal sarcoplasmic reticulum

Soluble tryptic peptides from the succinylated carboxymethylated protein

Biochem. J.

Primary structure of the calcium ion-transporting adenosine triphosphatase of rabbit skeletal sarcoplasmic reticulum

Soluble peptides from the chymotryptic digest of the carboxymethylated protein

Biochem. J.

Primary structure of the calcium ion-transporting adenosine triphosphatase from rabbit skeletal sarcoplasmic reticulum

Some peptic, thermolytic, tryptic and staphylococcal-proteinase peptides

Biochem. J.

The primary structure of the calcium ion-transporting adenosine triphosphatase protein of rabbit skeletal sarcoplasmic reticulum

Peptides derived from digestion with cyanogen bromide, and the sequences of three long extramembranous segments

Biochem. J.

Direct demonstration of structural changes in soluble, monomeric Ca2+ ATPase associated with Ca2+ release during the transport cycle

A rapid alkaline extraction procedure for screening recombinant plasmid DNA

Nucl. Acids Res.

Muscle contraction induced by exercise

A syndrome attributable to decreased relaxing factor

N. Eng. J. Med.

Energy interconversion by the Ca2+-dependent ATPase of the sarcoplasmic reticulum

Ann. Rev. Biochem.

pEMBL: a new family of single stranded plasmids

Nucl. Acids Res.

Article
Two Ca²⁺ ATPase genes: Homologies and mechanistic implications of deduced amino acid sequences

Direct demonstration of structural changes in soluble, monomeric Ca²⁺ ATPase associated with Ca²⁺ release during the transport cycle

Energy interconversion by the Ca²⁺-dependent ATPase of the sarcoplasmic reticulum