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Arginine kinase shows nucleoside diphosphate kinase-like activity toward deoxythymidine diphosphate

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Abstract

Arginine kinase (AK) (ATP: L-arginine phosphotransferase, E.C. 2.7.3.3) catalyzes the reversible transfer of ATP γ-phosphate group to L-arginine to synthetize phospho-arginine as a high-energy storage. Previous studies suggest additional roles for AK in cellular processes. Since AK is found only in invertebrates and it is homologous to creatine kinase from vertebrates, the objective of this work was to demonstrate nucleoside diphosphate kinase-like activity for shrimp AK. For this, AK from marine shrimp Litopenaeus vannamei (LvAK) was purified and its activity was assayed for phosphorylation of TDP using ATP as phosphate donor. Moreover, by using high-pressure liquid chromatography (HPLC) the phosphate transfer reaction was followed. Also, LvAK tryptophan fluorescence emission changes were detected by dTDP titration, suggesting that the hydrophobic environment of Trp 221, which is located in the top of the active site, is perturbed upon dTDP binding. The kinetic constants for both substrates Arg and dTDP were calculated by isothermal titration calorimetry (ITC). Besides, docking calculations suggested that dTDP could bind LvAK in the same cavity where ATP bind, and LvAK basic residues (Arg124, 126 and 309) stabilize the dTDP phosphate groups and the pyrimidine base interact with His284 and Ser122. These results suggest that LvAK bind and phosphorylate dTDP being ATP the phosphate donor, thus describing a novel alternate nucleoside diphosphate kinase-like activity for this enzyme.

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Acknowledgments

Jose Max Hernández-Flores was supported by a student fellowship from CONACyT (Mexico’s National Science and Research Council). Alonso A. Lopez-Zavala was supported by CONACyT under the grant “Fondo Consolidacion Institucional (I0007-2015-01, #250973)”. Also, authors acknowledge financial support from CONACyT grant CB-2009-131859. We acknowledge technical bibliographical support to Mr. Gerardo Reyna and technical support from Emmanuel Aispuro M.Sc. and Dr. Refugio Pérez from Univ. Sonora. Authors also thank Dr. Aldo Arvizu-Flores for help with the docking.

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Authors and Affiliations

  1. Departamento de Ciencias Químico Biológicas, Universidad de Sonora, Calle Rosales y Blvd. Luis Encinas s/n, Col. Centro, Hermosillo, Sonora, 83000, México

    Alonso A. Lopez-Zavala & Rocio Sugich-Miranda

  2. Biomolecular Structure Laboratory, Centro de Investigación en Alimentación y Desarrollo, A.C. (CIAD), Carretera a Ejido La Victoria Km 0.6, Apartado Postal 1735, Hermosillo, Sonora, 83304, México

    Rogerio R. Sotelo-Mundo, Jose M. Hernandez-Flores, Maria E. Lugo-Sanchez & Karina D. Garcia-Orozco

Authors
  1. Alonso A. Lopez-Zavala
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  2. Rogerio R. Sotelo-Mundo
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  3. Jose M. Hernandez-Flores
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  4. Maria E. Lugo-Sanchez
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  5. Rocio Sugich-Miranda
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  6. Karina D. Garcia-Orozco
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Corresponding author

Correspondence to Karina D. Garcia-Orozco.

Electronic supplementary material

Molecular weight and quaternary structure determination of LvAK

Quaternary structure of shrimp LvAK was determined by gel filtration chromatography using a Superdex 200 column (GE Healthcare, USA) with an approximate column volume of 23 mL. The column was previously equilibrated with three column volumes of running buffer (20 mM sodium phosphate pH 7.5 and 200 mM NaCl) and then calibrated with molecular weight standards: albumin (66 kDa), ovalbumin (44 kDa) and inhibitor soybean trypsin (21.5 kDa). LvAK was dialyzed with running buffer and 250 μl were applied to the column. Fractions were collected and enzymatic activity was measured. The molecular weight was calculated by linear regression using elution time of standards as references. The peaks containing enzymatic activity were analyzed by SDS-PAGE as described above.

Determination of the native molecular weight of native shrimp AK

In order to determine the shrimp AK (LvAK) quaternary structure, the purified enzyme was separated by size-exclusion chromatography using a Superdex 200 column. Linear regression analysis of the data indicates that LvAK has a native molecular weight of 38 kDa (Fig. 1, panel A). This value agrees with the calculated value obtained from the amino acid sequence (≈40.16 kDa) using the ProtParam algorithm (Wilkins et al. 1999). Also, the fractions corresponding to the monomer have a molecular mass of 40 kDa by SDS-PAGE (Fig. 1, panel B). The slight difference in values may be due to the shape of the protein but size-exclusion chromatography demonstrate that shrimp AK is a monomeric enzyme. Other monomeric AKs are those of mollusks and arthropods such as the oyster Crassostrea virginica, the worm Manduca sexta and the cockroach Periplaneta americana, whose molecular weights are about 40 kDa (Brown and Grossman 2004; Fujimoto et al. 2005; Rosenthal et al. 1977). Dimeric invertebrate AKs are less common, such as the sea cucumber Stichopus japonicus and sea anemone Anthopleura japonicus, which are dimeric and have an approximate weight of 80 kDa (Guo et al. 2003; Suzuki et al. 1997).

Figure S1

Gel filtration chromatography using a Superdex 200 column. Panel A) The molecular weight standards were albumin (66 kDa), ovalbumin (44 kDa) and soybean trypsin (21.5 kDa) and are shown as dotted lines?. LvAK is shown as a solid line. Inset shows the calibration graph. Panel B) SDS-PAGE of fractions from gel filtration. LvAK has a molecular weight of 40 kDa. The lane indicated by an asterisk (*) correspond to the fraction 16, which is the peak of the chromatography. (GIF 452 kb)

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Lopez-Zavala, A.A., Sotelo-Mundo, R.R., Hernandez-Flores, J.M. et al. Arginine kinase shows nucleoside diphosphate kinase-like activity toward deoxythymidine diphosphate. J Bioenerg Biomembr 48, 301–308 (2016). https://doi.org/10.1007/s10863-016-9660-1

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  • DOI: https://doi.org/10.1007/s10863-016-9660-1

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