Parasites, Hosts and Diseases

The Korea Society for Parasitology and Tropical Medicine (대한기생충학·열대의학회)
권호 표지
DOI QR코드

DOI QR Code

Phosphagen Kinases of Parasites: Unexplored Chemotherapeutic Targets

  • Jarilla, Blanca R. (Department of Environmental Health Sciences, Kochi Medical School) ;
  • Agatsuma, Takeshi (Department of Immunology, Research Institute for Tropical Medicine)
  • Received : 2010.07.28
  • Accepted : 2010.08.28
  • Published : 2010.12.31
Download PDF
⟨ Previous Next ⟩

Abstract

Due to the possible emergence of resistance and safety concerns on certain treatments, development of new drugs against parasites is essential for the effective control and subsequent eradication of parasitic infections. Several drug targets have been identified which are either genes or proteins essential for the parasite survival and distinct from the hosts. These include the phosphagen kinases (PKs) which are enzymes that playa key role in maintenance of homeostasis in cells exhibiting high or variable rates of energy turnover by catalizing the reversible transfer of a phosphate between ATP and naturally occurring guanidine compounds. PKs have been identified in a number of important human and animal parasites and were also shown to be significant in survival and adaptation to stress conditions. The potential of parasite PKs as novel chemotherapeutic targets remains to be explored.

Keywords

References

  1. Wyss M, Smeitink J, Wevers RA, Wallimann T. Mitochondrial creatine kinase: a key enzyme of aerobic energy metabolism. Biochim Biophys Acta 1992; 1102: 119-166. https://doi.org/10.1016/0005-2728(92)90096-K
  2. Ellington WR. Evolution and physiological roles of phosphagen systems. Annu Rev Physiol2001; 63: 289-325. https://doi.org/10.1146/annurev.physiol.63.1.289
  3. Morrison JF. Arginine kinase and other invertebrate guanidine kinases. In Boyer PC, ed, The Enzymes. New York, USA. Academic Press. 1973, p 457-486.
  4. Robin Y. Phosphagens and molecular evolution in worms. Bio-Systems 1974; 6: 49-56. https://doi.org/10.1016/0303-2647(74)90010-0
  5. Thoai VN. Homologous phosphagen phosphokinases. In Thoai VN, Roche J, eds, Homologous Enzymes and Biochemical Evolution. New York, USA. Gordon and Breach. 1968, p 199-229.
  6. Wallimann T, Wyss M, Brdiczka D, Nicolay K, Eppenberger HM. Intracellular compartmentation, structure and function of creatine kinase isoenzymes in tissues with high and fluctuating energy demands: the 'phosphocreatine drcuit' for cellular energy homeostasis. Biochem J 1992; 281: 21-40. https://doi.org/10.1042/bj2810021
  7. Sauer U, Schlattner U. Inverse metabolic engineering with phosphagen kinase systems improves the cellular energy state. Metab Eng 2004; 6: 220-228. https://doi.org/10.1016/j.ymben.2003.11.004
  8. Goil MM. Study of phosphagen in two trematodes. Z Parasitenkd 1980; 61: 271-275. https://doi.org/10.1007/BF00925518
  9. Pereira CA, Alonso GD, Paveto Me, Iribarren A, Cabanas ML, Torres HN, Flawia MM. Trypanosma cruzi arginine kinase characterization and cloning. A novel energetic pathway in protowan parasites. J Bioi Chem 2000; 275: 1495-1501. https://doi.org/10.1074/jbc.275.2.1495
  10. Pereira CA, Alonso GD, lvaldi MS, Silber AM, Alves MJM, Bouvier lA, Flawia MM, Torres HN. Arginine metabolism in Tryparwsoma cruzi is coupled to parasite stage and replication. FEBS Lett 2002; 526: 111-114. https://doi.org/10.1016/S0014-5793(02)03157-5
  11. Uda K, Fujimoto N, Akiyama Y, Mizuta K Tanaka K, Ellington WR Suzuki T. Evolution of the arginine kinase family. Comp Biochem Physiol Part D Genomics Proteomics 2006; 1: 209-218. https://doi.org/10.1016/j.cbd.2005.10.007
  12. Alonso GD, Pereira CA, Remedi MS, Paveto Me, Cochella L, Ivaldi MS, Gerez de Burgos NM, Torres HN, Flawia MM. Arginine kinase of the flagellate protozoa Trypanosoma cruzi: regulation of its expression and catalytic activity. PEES Lett 2001; 498: 22-25.
  13. Miranda MR, Canepa GE, Bouvier LA, Pereira CA. Trwanosoma cruzi: oxidative stress induces arginine kinase expression. Exp Parasitol 2006; 114: 341-344. https://doi.org/10.1016/j.exppara.2006.04.004
  14. Pereira CA, Alonso GD, Ivaldi S, Bouvier LA, Torres HN, Flawia MM. Screening of substrate analogs as potential enzyme inhibitors for the arginine kinase of Trypanosoma cruzi. J Eukaryot Microbiol 2003; 50: 132-134. https://doi.org/10.1111/j.1550-7408.2003.tb00247.x
  15. Canonaco F, Schlattner U, Pruett PS, Wallimann T, Sauer U. Functional expression of phosphagen kinase systems confers resistance to transient stresses in Saccharomyces cerevisiae by buffering the ATP pool. J Bioi Chem 2002; 277: 31303-31309. https://doi.org/10.1074/jbc.M204052200
  16. Canonaco F, Schlattner U, Wallimann T, Sauer U. Functional expression of arginine kinase improves recovery from pH stress of Escherichia coli. Biotechnol Lett 2003; 25: 1013-1017. https://doi.org/10.1023/A:1024172518062
  17. Livingstone DR, Dezwaan A, Leopold M, Marteijn E. Studies on the phylogenetic distribution of pyruvate oxidoreductases. Biochem Syst Ecol 1983; 11: 415-425. https://doi.org/10.1016/0305-1978(83)90047-9
  18. Thompson SN, Platzer EG, Lee RW. Phosphoarginine-adenosine triphosphate exchange detected in vivo in a microscopic nematode parasite by flow 31P FT-NMR spectroscopy. Magn Reson Med 1992; 28: 311-317. https://doi.org/10.1002/mrm.1910280213
  19. Platzer EG, Wang W, Thompson SN, Borchardt DB. Arginine kinase and phosphoarginine, a functional phosphagen, in the rhabditoid nematode Steinemema carpocapsae. J Parasitol 1999; 85: 603-607. https://doi.org/10.2307/3285730
  20. Wickramasinghe S, Uda K, Nagataki M, Yatawara L, Rajapakse RPVJ, Watanabe Y, Suzuki T, Agatsuma T. Toxocara canis: Molecular doning, characterization, expression and comparison of the kinetics of cDNA-derived arginine kinase. Exp Parasitol 2007; 117: 124-132. https://doi.org/10.1016/j.exppara.2007.03.015
  21. Nagataki M, Wickramasinghe S, Uda K, Suzuki T, Yano H, Watanabe Y, Agatsuma T. Cloning and enzyme activity of a recombinant phosphagen kinase from nematodes (in Japanese). Jpn J Med Technol 2008; 57: 41-45.
  22. Matthews BF, MacDonald MH, Thai VK, Tucker ML. Molecular characterization of arginine kinases in the soybean cyst nematode (Heterodera glycines). J Nematol 2003; 35, 252-258.
  23. Stein LD, Harn DA, David JR A cloned ATP: guanidine kinase in the trematode Schistosma mansoni has a novel duplicated structure. J Biol Chem 1990; 265: 6582-6588.
  24. Shoemaker CB. The Schistosoma mansoni phosphagen kinase gene contains two dosely apposed transcription initiation sites and arose from a fused gene duplication. Mol Biochem Parasitol 1994; 68: 319-322. https://doi.org/10.1016/0166-6851(94)90177-5
  25. Awama AM, Paracuellos P, Laurent S, Dissous C, Marcillat O, Gouet P. Crystallization and X-ray analysis of the Schistosoma mansoni guanidine kinase. Acta Crystallogr Sect F Struct Biol Cryst Commun 2008; 64: 854-857. https://doi.org/10.1107/S1744309108025979
  26. Jarilla BR, Tokuhiro S, Nagataki M, Hong SJ, Uda K, Suzuki T, Agatsuma T. Molecular cloning and characterization of a novel two-domain taurocyamine kinase from the lung fluke Paragonimus westermani. FEBS Lett 2009; 583: 2218-2224. https://doi.org/10.1016/j.febslet.2009.05.049
  27. Stein LD, Ham DA, David JR A cloned ATP: guanidine kinase in the trematode Schistosma mansoni has a novel duplicated structure. J Biol Chem 1990; 265: 6582-6588.
  28. Uda K, Saishoji N, Ichinari S, Ellington WR, Suzuki T. Origin and properties of cytoplasmic and mitochondrial isoforms of taurocyamine kinase. FEBS J 2005; 272: 3521-3530. https://doi.org/10.1111/j.1742-4658.2005.04767.x
  29. Compaan DM, Ellington WR. Functional consequences of a gene duplication and fusion event in an arginine kinase. J Exp Biol 2003; 206: 1545-1556. https://doi.org/10.1242/jeb.00299
  30. Suzuki T, Tomoyuki T, Uda K. Kinetic properties and structural characteristics of an unusual two-domain arginine kinase from the dam Corbicula japonica. FEBS Lett 2003; 533: 95-98. https://doi.org/10.1016/S0014-5793(02)03765-1
  31. Suzuki T, Kawasaki Y, Furukohri T, Ellington WR Evolution of phosphagen kinase. VI. Isolation, characterization and eDNAderived amino acid sequence oflombricine kinase from the earthworm Eisenia foetida, and identification of a possible candidate for the guanidine substrate recognition site. Biochim Biophys Acta 1997; 1343: 152-159. https://doi.org/10.1016/S0167-4838(97)00128-3
  32. Keiser J, Utzinger J. Food-borne trematodiasis: current chemotherapy and advances with artemisinins and synthetic trioxolanes. Trends Parasitol 2007; 23: 555-562
  33. Nwaka S, Ramirez B, Brun R, Maes L, Douglas F, Ridley R Advancing drug innovation for neglected diseases-criteria for lead progression. PLoS Negl Trop Dis 2009; 3: e440. https://doi.org/10.1371/journal.pntd.0000440
  34. Cavalli A, Bolognesi ML. Neglected tropical diseases: Multi-Target-Directed ligands in the search for novel lead candidates against Trypanosoma and Leishmania. J Med Chern 2009; 52: 7339-7359. https://doi.org/10.1021/jm9004835
  35. Krasky A, Rohwer A, Schroeder J. Selzer PM. A combined bioinformatics and chemoinformatics approach for the development of new antiparasitic drugs. Genomics 2007; 89: 36-43. https://doi.org/10.1016/j.ygeno.2006.09.008
  36. Fernandez P, Haouz A, Pereira CA, Aguilar C, Alzari PM. The crystal structure of Trypanosoma cruzi arginine kinase. Proteins 2007; 69: 209-212. https://doi.org/10.1002/prot.21557
  37. Silber AM, Colli W, Ulrich H, Alves MJM, Pereira CA Amino acid metabolic routes in Trypanosoma cruzi: Possible therapeutic targets against Chagas' disease. Curr Drug Targets Infect Disord 2005; 5: 53-64. https://doi.org/10.2174/1568005053174636
  38. Paveto C, Guida MC, Esteva MI, Martino V, Coussio J, Flawia MM, Torres HN. Anti-Trypanosoma cruzi activity of green tea (Camellia sinensis) catechins. Antimicrob Agents Chemother 2004; 48: 69- 74. https://doi.org/10.1128/AAC.48.1.69-74.2004
  39. Wu XA, Zhu WJ, Lu ZR, Xia Y, Yang JM, Zou F, Wang XY. The effect of rutin on arginine kinase: inhibition kinetics and thermodynamics merging with docking simulation. Int J Bioi Macromol 2009; 44: 149-155. https://doi.org/10.1016/j.ijbiomac.2008.11.007
  40. Wickramasinghe S, Yatawara L, Nagataki M, Takamoto M, Watanabe Y, Rajapakse RPVJ, Uda K, Suzuki T, Agatsuma T. Development of a highly sensitive IgG-ELISA based on recombinant arginine kinase of Toxocara canis for serodiagnosis of visceral larva migrans in the murine model. Parasitol Res 2008; 103: 853-858. https://doi.org/10.1007/s00436-008-1067-4

Cited by

  1. Arginine kinase of the sheep blowfly Lucilia cuprina: Gene identification and characterization of the native and recombinant enzyme vol.102, pp.2, 2010, https://doi.org/10.1016/j.pestbp.2011.12.001
  2. 동양달팽이(Nesiohelix samarangae)의 arginine kinase 유전자 분석 및 발현 패턴에 관한 연구 vol.29, pp.3, 2010, https://doi.org/10.9710/kjm.2013.29.3.171
  3. Molecular Cloning and Characterization of Taurocyamine Kinase from Clonorchis sinensis : A Candidate Chemotherapeutic Target vol.7, pp.11, 2010, https://doi.org/10.1371/journal.pntd.0002548
  4. Arginine kinase in Toxocara canis: Exon-intron organization, functional analysis of site-directed mutants and evaluation of putative enzyme inhibitors vol.9, pp.10, 2016, https://doi.org/10.1016/j.apjtm.2016.07.023
  5. In-Depth Proteomic Analysis of the Porcine Retina by Use of a four Step Differential Extraction Bottom up LC MS Platform vol.54, pp.9, 2017, https://doi.org/10.1007/s12035-016-0172-0
  6. Natural Products Containing ‘Rare’ Organophosphorus Functional Groups vol.24, pp.5, 2010, https://doi.org/10.3390/molecules24050866
  7. Apoferritin and Apoferritin-Capped Metal Nanoparticles Inhibit Arginine Kinase of Trypanosoma brucei vol.25, pp.15, 2010, https://doi.org/10.3390/molecules25153432
  8. Characterisation of arginine kinase intron regions and their potential as molecular markers for population genetic studies of Bithynia snails (Gastropoda: Bithyniidae) in Thailand vol.40, pp.4, 2010, https://doi.org/10.1080/13235818.2020.1794294