Skip to main content
SpringerLink
Log in

Isolation and characterization of an adenylate kinase from the lateral muscle of bastard halibut Paralichthys olivaceus

  • Original Article
  • Chemistry and Biochemistry
  • Published:
Fisheries Science Aims and scope Submit manuscript

Abstract

Adenylate kinase (ATP:AMP phosphotransferase, EC 2.7.4.3) (AK) is the enzyme that catalyzes the reversible conversion of MgATP + AMP to MgADP + ADP, a principal step in adenine nucleotide metabolism and cellular energy homeostasis. To enrich the information about fish AKs, we isolated this enzyme from the lateral muscle of bastard halibut Paralichthys olivaceus and biochemically characterized it. The halibut enzyme (PoAK) extracted from the lateral muscle was purified by column chromatographies on TOYOPEARL SP-650 M and Superdex 75 10/300. The purified PoAK showed a single protein band of ~ 22 kDa on SDS–polyacrylamide gel electrophoresis, and optimal temperature and pH at around 40 °C and 7, respectively. PoAK was appreciably heat stable, e.g., the temperature that caused 50% inactivation during 30-min incubation was 54 °C. The molar ratio for ATP:ADP:AMP in the equilibrium state of the reaction was ~ 1:1:1. Peptide mass fingerprinting indicated that PoAK is the product of adenylate kinase isoform 1 gene (GenBank, XP_019937160.1) encoded in the halibut genome. The deduced amino-acid sequence of the halibut AK comprised 194 residues and showed 92, 91 and 81% amino-acid identities to those of a putative rainbow trout AK, a carp AK and a chicken AK, respectively.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  • Atkinson DE (1968) Energy charge of the adenylate pool as a regulatory parameter. Interaction with feedback modifiers. Biochem 7:4030–4034

    Article  CAS  Google Scholar 

  • Atkinson DE, Walton GM (1967) Adenosine triphosphate conservation in metabolic regulation rat liver citrate cleavage enzyme. J Biol Chem 242:3239–3241

    CAS  PubMed  Google Scholar 

  • Ayabe T, Park SK, Takenaka H, Takenaka O, Maruyama H, Sumida M, Onitsuka T, Hamada M (2000) The steady-state kinetics of the enzyme reaction tested by site-directed mutagenesis of hydrophobic residues (Val, Leu, and Cys) in the C-terminal α-helix of human adenylate kinase. J Biochem 128:181–187

    Article  CAS  Google Scholar 

  • Baker JS, McCormick MC, Robergs RA (2010) Interaction among skeletal muscle metabolic energy systems during intense exercise. J Nutr Metab 2010:905612

    Article  Google Scholar 

  • Bendall JR, Swatland HJ (1988) A review of the relationship of pH with physical aspects of pork quality. Meat Sci 24:85–96

    Article  CAS  Google Scholar 

  • Bosworth IVCA, Chou CW, Cole RB, Rees BB (2005) Protein expression patterns in zebrafish skeletal muscle: initial characterization and the effects of hypoxic exposure. Proteomics 5:1362–1371

    Article  CAS  Google Scholar 

  • Briskey EJ (1964) Etiological status and associated studies of pale, soft, exudative porcine musculature. In: Chichester CO, Mrak EM, Stewart GF (eds) Advances in Food Research, vol 13. Academic Press, New York, pp 89–178

    Google Scholar 

  • Chapman AG, Fall L, Atkinson DE (1971) Adenylate energy charge in Escherichia coli during growth and starvation. J Bacteriol 108:1072–1086

    Article  CAS  Google Scholar 

  • Chauhan SS, England EM (2018) Postmortem glycolysis and glycogenolysis: insights from species comparisons. Meat Sci 114:118–126

    Article  Google Scholar 

  • Colowick SP, Kalckar HM (1943) The role of myokinase in transphosphorylations. J Biol Chem 148:314

    Google Scholar 

  • Dzeja P, Terzic A (2009) Adenylate kinase and AMP signaling networks: metabolic monitoring, signal communication and body energy sensing. Int J Mol Sci 10:1729–1772

    Article  CAS  Google Scholar 

  • England EM, Scheffler TL, Kasten SC, Matarneh SK, Gerrard DE (2013) Exploring the unknowns involved in the transformation of muscle to meat. Meat Sci 95:837–843

    Article  CAS  Google Scholar 

  • England EM, Matarneh SK, Scheffler TL, Wachet C, Gerrard DE (2015) Altered AMP deaminase activity may extend postmortem glycolysis. Meat Sci 102:8–14

    Article  CAS  Google Scholar 

  • Fruscione F, Sturia L, Duncan G, Van Etten JL, Valbuzzi P, De Flora A, Di Zanni E, Tonetti M (2008) Differential role of NADP+ and NADPH in the activity and structure of GDP-D-mannose 4, 6-dehydratase from two chlorella viruses. J Biol Chem 283:184–193

    Article  CAS  Google Scholar 

  • Fukushima M, Hayashi S, Ooshiro Z (1974) Studies on myokinase in the muscle of fishes-II. Some properties of myokinase isozymes purifies from muscle of carp. Bull Jap Soc Sci Fish 40:299–302

    Article  CAS  Google Scholar 

  • Gornall AG, Bardawill CJ, David MM (1949) Determination of serum proteins by means of the biuret reaction. J Biol Chem 177:751–766

    CAS  PubMed  Google Scholar 

  • Iwamoto M, Ioka H, Saito M, Yamanaka H (1985) Relation between rigor mortis of sea bream and storage temperature. Bull Jap Soc Fish Sci 51:443

    Article  CAS  Google Scholar 

  • Iwamoto M, Yamanaka H, Abe H, Ushio H, Watabe S, Hashimoto K (1988) ATP and creatine phosphate breakdown in spiked plaice muscle during storage, and activities of some enzymes involved. J Food Sci 53:1662–1665

    Article  CAS  Google Scholar 

  • Kalckar HM (1943) The role of myokinase in transphosphorylations II. The enzymatic action of myokinase on adenine nucleotides. J Bio Chem 148:127–137

    CAS  Google Scholar 

  • Konno Y, Konno K (2014) Myosin denaturation in “burnt” bluefin tuna meat. Fish Sci 80:381–388

    Article  CAS  Google Scholar 

  • Kuby SA (1990) A study of enzymes. CRC Press, Boca Raton

    Google Scholar 

  • Kyrana VR, Lougovois VP, Valsamis DS (1997) Assessment of shelf-life of maricultured gilthead sea bream (Sparus aurata) stored in ice. Int J Food Sci Technol 32:339–347

    Article  CAS  Google Scholar 

  • Lowry OH, Rosebrough NJ, Farr AL, Randall RJ (1951) Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275

    CAS  PubMed  Google Scholar 

  • Milan D, Woloszyn N, Yerle M, Roy PL, Bonnet M, Riquet J, Lahbib-Mansais Y, Caritez JC, Robic A, Sellier P, Elsen JM, Gellin J (1996) Accurate mapping of the “acid meat” RN gene on genetic and physical maps of pig chromosome 15. Mamm Genome 7:47–51

    Article  CAS  Google Scholar 

  • Minami S, Sato M, Shiraiwa Y, Iwamoto K (2011) Molecular characterization of adenosine 5’-monophosphate deaminase—the key enzyme responsible for the umami taste of nori (Porphyra yezoensis Ueda, Rhodophyta). Mar Biotechnol 13:1140

    Article  CAS  Google Scholar 

  • Mora DA, Hamada Y, Okamoto A, Tateishi A, Tachibana K (2007) Characteristics of burnt meat in cultured yellowtail Seriola quinqueradiata. Jap Soc Fish Sci 73:651–659

    Article  CAS  Google Scholar 

  • Noda L (1973) Adenylate kinase. In: Boyer PD (ed) The enzymes, Academic Press, New York.

  • Noda L, Schulz GE, von Zabern I (1975) Crystalline adenylate kinase from carp muscle. Eur J Biochem 51:229–235

    Article  CAS  Google Scholar 

  • Ocaño-Higuera VM, Marquez-Ríos E, Canizales-Dávila M, Castillo-Yáñez FJ, Pacheco-Aguilar R, Lugo-Sánchez ME, Graciano-Verdugo AZ (2009) Postmortem changes in cazon fish muscle stored on ice. Food Chem 116:933–938

    Article  Google Scholar 

  • Oliver IT (1955) A spectrophotometric method for the determination of creative phosphokinase and myokinase. Biochem J 61:116

    Article  CAS  Google Scholar 

  • Ooshiro Z, Fukushima M, Hayashi S (1974) Studies on myokinase in the muscle of fishes.I. Isolation and purification of myokinase isozymes from muscle of carp. Bull Jap Soc Fish Sci 40:291–298

    Article  CAS  Google Scholar 

  • Panayiotou C, Solaroli N, Karlsson A (2014) The many isoforms of human adenylate kinases. Int J Biochem Cell Biol 49:75–83

    Article  CAS  Google Scholar 

  • Porzio MA, Pearson AM (1977) Improved resolution of myofibrillar proteins with sodium dodecyl sulfate-polyacrylamide gel electrophoresis. Biochim Biophys Acta 490:27–34

    Article  CAS  Google Scholar 

  • Rammouz REl, Berri C, Bihan-Duval EL, Babilé R, Fernandez X (2004) Breed differences in the biochemical determinism of ultimate pH in breast muscles of broiler chickens—a key role of AMP deaminase? Pault Sci 83:1445–1451

    Article  Google Scholar 

  • Ryder JM, Buisson DH, Scott DN, Fletcher GC (1984) Storage of New Zealand jack mackerel (Trachurus novaezelandiae) in ice: chemical, microbiological and sensory assessment. J Food Sci 49:1453–1456

    Article  CAS  Google Scholar 

  • Saito T, Arai K, Matsuyoshi M (1959) A new method for estimating the freshness of fish. Bull Jap Soc Fish Sci 24:749–750

    Article  CAS  Google Scholar 

  • Scheffler TL, Gerrard DE (2007) Mechanisms controlling pork quality development: the biochemistry controlling postmortem energy metabolism. Meat Sci 77:7–16

    Article  CAS  Google Scholar 

  • Seki H, Nakazato K, Hamada-Sato N (2017) Adenosine monophosphate degradation and inosinic acid accumulation in the shrimp Penaeus japonicus. Int Aqua Res 9:37–52

    Article  Google Scholar 

  • Thiede B, Höhenwarter W, Krah A, Mattow J, Schmid M, Schmidt F, Jungblut PR (2005) Peptide mass fingerprinting. Methods 35:237–247

    Article  CAS  Google Scholar 

  • Vincent A, Blair JM (1970) The coupling of the adenylate kinase and creatine kinase equilibria. Calculation of substrate and feedback signal levels in muscle. FEBS Lett 7:239–244

    Article  CAS  Google Scholar 

  • Yoneya T, Okajima T, Tagaya M, Tanizawa K, Fukui T (1990) The role of Leu-190 in the function and stability of adenylate kinase. J Biol Chem 265:21488–21493

    CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Laboratory of Marine Biotechnology and Microbiology, Division of Marine Life Sciences, Faculty of Fisheries Sciences, Hokkaido University, Hakodate, Hokkaido, 041-8611, Japan

    Kenta Arai, Akira Inoue & Takao Ojima

Authors
  1. Kenta Arai
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Akira Inoue
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Takao Ojima
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Takao Ojima.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Arai, K., Inoue, A. & Ojima, T. Isolation and characterization of an adenylate kinase from the lateral muscle of bastard halibut Paralichthys olivaceus. Fish Sci 86, 385–394 (2020). https://doi.org/10.1007/s12562-019-01393-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12562-019-01393-1

Keywords

Search

Navigation