Suzuki T et al. (2000), Stichopus japonicus arginine kinase: gene struc...

ECB-ART-37586

Biochem J 2000 Nov 01;351 Pt 3:579-85.

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Stichopus japonicus arginine kinase: gene structure and unique substrate recognition system.

Suzuki T , Yamamoto Y , Umekawa M .

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Arginine kinase from the sea cucumber Stichopus japonicus underwent a unique molecular evolution. Unlike the monomeric 40 kDa arginine kinases from molluscs and arthropods, Stichopus arginine kinase is dimeric, the same as cytoplasmic isoenzymes of the vertebrate creatine kinases. Its entire amino acid sequence is more similar to creatine kinases than to other arginine kinases, but the guanidino specificity region (GS region) is of the arginine kinase type. To elucidate its unusual evolution, the structure of the Stichopus arginine kinase gene was determined. It consisted of seven exons and six introns, and a part of the exon 2 of the Stichopus gene corresponds to the GS region. Compared with the structure of the human muscle creatine kinase gene (seven exons, six introns), the splice junctions of five introns were conserved exactly between the two genes, suggesting that these introns had been conserved for at least 500 million years. The entire sequence of Stichopus arginine kinase is distinctly included in the creatine kinase cluster in all tree construction methods examined. On the other hand, if the tree is constructed only from sequences corresponding to Stichopus exon 2, it is placed in the arginine kinase cluster. Thus we conclude that Stichopus arginine kinase evolved not from the arginine kinase gene but from the creatine kinase gene, and suggest that its GS region, determining substrate specificity, has been replaced by an arginine kinase type via exon shuffling. In typical arginine kinases four residues, Ser(63), Gly(64), Val(65) and Tyr(68) (numbering from the Limulus polyphemus sequence), in the GS region are highly conserved and are associated with substrate binding. Among them, Tyr(68) appears to play a crucial role by forming a hydrogen bond with the substrate, and is conserved exactly in all arginine kinases. However, in Stichopus arginine kinase, none of these four conserved residues were present. Nevertheless, the enzyme displays an affinity for the substrate arginine (K(m)=0.8 mM) comparable with other arginine kinases. This implies that a completely different substrate-binding system has been developed in Stichopus arginine kinase. We propose that the His(64) in Stichopus arginine kinase acts as a substitute for the Tyr(68) in other arginine kinases, and that the imidazole ring of His(64) is hydrogen bonded with the substrate arginine, thus stabilizing it.

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Genes referenced: LOC100887844 pus1 srpl

References [+] :

Ellington, Phosphocreatine represents a thermodynamic and functional improvement over other muscle phosphagens. 1989, Pubmed

Ellington, Phosphocreatine represents a thermodynamic and functional improvement over other muscle phosphagens. 1989, Pubmed
Fritz-Wolf, Structure of mitochondrial creatine kinase. 1996, Pubmed
Goodman, An evolutionary tree for invertebrate globin sequences. 1988, Pubmed
Haas, Isolation and characterization of the gene and cDNA encoding human mitochondrial creatine kinase. 1989, Pubmed
Kenyon, Creatine kinase: structure-activity relationships. 1983, Pubmed
Mühlebach, Sequence homology and structure predictions of the creatine kinase isoenzymes. 1994, Pubmed
Mühlebach, Evolution of the creative kinases. The chicken acidic type mitochondrial creatine kinase gene as the first nonmammalian gene. 1996, Pubmed
Pineda, Structural and functional implications of the amino acid sequences of dimeric, cytoplasmic and octameric mitochondrial creatine kinases from a protostome invertebrate. 1999, Pubmed
Rogers, Exon shuffling and intron insertion in serine protease genes. 1985, Pubmed
Stewart, Adaptive evolution in the stomach lysozymes of foregut fermenters. 1987, Pubmed
Strong, Isolation and sequence analysis of the gene for arginine kinase from the chelicerate arthropod, Limulus polyphemus: insights into catalytically important residues. 1995, Pubmed
Suzuki, Arginine kinase from Nautilus pompilius, a living fossil. Site-directed mutagenesis studies on the role of amino acid residues in the Guanidino specificity region. 2000, Pubmed
Suzuki, Evolution of phosphagen kinase. Primary structure of glycocyamine kinase and arginine kinase from invertebrates. 1994, Pubmed
Suzuki, Evolution of phosphagen kinase. Isolation, characterization and cDNA-derived amino acid sequence of two-domain arginine kinase from the sea anemone Anthopleura japonicus. 1997, Pubmed
Suzuki, Evolution of phosphagen kinase. VI. Isolation, characterization and cDNA-derived amino acid sequence of lombricine kinase from the earthworm Eisenia foetida, and identification of a possible candidate for the guanidine substrate recognition site. 1997, Pubmed
Suzuki, Gene duplication and fusion have occurred frequently in the evolution of phosphagen kinases--a two-domain arginine kinase from the clam Pseudocardium sachalinensis. 1998, Pubmed
Suzuki, Arginine kinase evolved twice: evidence that echinoderm arginine kinase originated from creatine kinase. 1999, Pubmed , Echinobase
Trask, Developmental regulation and tissue-specific expression of the human muscle creatine kinase gene. 1988, Pubmed
Zhou, Transition state structure of arginine kinase: implications for catalysis of bimolecular reactions. 1998, Pubmed