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Characterization of xanthine dehydrogenase and aldehyde oxidase of Marsupenaeus japonicus and their response to microbial pathogen

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Abstract

Reactive oxygen species (ROS) play key roles in many physiological processes. In particular, the sterilization mechanism of bacteria using ROS in macrophages is a very important function for biological defense. Xanthine dehydrogenase (XDH) and aldehyde oxidase (AOX), members of the molybdo-flavoenzyme subfamily, are known to generate ROS. Although these enzymes occur in many vertebrates, some insects, and plants, little research has been conducted on XDHs and AOXs in crustaceans. Here, we cloned the entire cDNA sequences of XDH (MjXDH: 4328 bp) and AOX (MjAOX: 4425 bp) from Marsupenaeus japonicus (kuruma shrimp) using reverse transcriptase-polymerase chain reaction (RT-PCR) and random amplification of cDNA ends (RACE). Quantitative real-time RT-PCR transcriptional analysis revealed that MjXDH mRNA is highly expressed in heart and stomach tissues, whereas MjAOX mRNA is highly expressed in the lymphoid organ and intestinal tissues. Furthermore, expression of MjAOX was determined to be up-regulated in the lymphoid organ in response to Vibrio penaeicida at 48 and 72 h after injection; in contrast, hydrogen peroxide (H2O2) concentrations increased significantly at 6, 12, 48, and 72 h after injection with white spot syndrome virus (WSSV) and at 72 h after injection with V. penaeicida. To the best of our knowledge, this study is the first to have identified and cloned XDH and AOX from a crustacean species.

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References

  1. Valko M, Leibfritz D, Moncol J, Cronin MT, Mazur M, Telser J (2007) Free radicals and antioxidants in normal physiological functions and human disease. Int J Biochem Cell Biol 39(1):44–84. https://doi.org/10.1016/j.biocel.2006.07.001

    Article  PubMed  CAS  Google Scholar 

  2. Cohn CA (2005) Quantifying hydrogen peroxide in iron-containing solutions using leuco crystal violet. Geochem Trans 6(3):47. https://doi.org/10.1063/1.1935449

    Article  PubMed Central  CAS  Google Scholar 

  3. Graves JA, Metukuri M, Scott D, Rothermund K, Prochownik EV (2008) Regulation of reactive oxygen species homeostasis by peroxiredoxins and c-Myc. J Biol Chem 284(10):6520–6529. https://doi.org/10.1074/jbc.m807564200

    Article  PubMed  Google Scholar 

  4. Chelikani P, Fita I, Loewen PC (2004) Diversity of structures and properties among catalases. Cell Mol Life Sci 61(2):192–208. https://doi.org/10.1007/s00018-003-3206-5

    Article  PubMed  CAS  Google Scholar 

  5. Nordberg J, Arnér ESJ (2001) Reactive oxygen species, antioxidants, and the mammalian thioredoxin system. Free Radic Biol Med 31:1287–1312

    Article  PubMed  CAS  Google Scholar 

  6. Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70:158–169

    PubMed  CAS  Google Scholar 

  7. Juven BJ, Pierson MD (1996) Antibacterial effects of hydrogen peroxide and methods for its detection and quantitation. J Food Prot 59(11):1233–1241. https://doi.org/10.4315/0362-028x-59.11.1233

    Article  CAS  Google Scholar 

  8. Skulachev VP (1998) Possible role of reactive oxygen species in antiviral defense. Biochem 63:1438–1440

    CAS  Google Scholar 

  9. Iwanaga S, Lee B (2005) Recent advances in the innate immunity of invertebrate animals. BMB Rep 38(2):128–150. https://doi.org/10.5483/bmbrep.2005.38.2.128

    Article  CAS  Google Scholar 

  10. Lavine M, Strand M (2002) Insect hemocytes and their role in immunity. Insect Biochem Mol Biol 32(10):1295–1309. https://doi.org/10.1016/s0965-1748(02)00092-9

    Article  PubMed  CAS  Google Scholar 

  11. Manevski N, Balavenkatraman KK, Bertschi B, Swart P, Walles M, Camenisch G, Litherland K (2014) Aldehyde oxidase activity in fresh human skin. Drug Metab Dispos 42(12):2049–2057. https://doi.org/10.1124/dmd.114.060368

    Article  PubMed  CAS  Google Scholar 

  12. Pope SD, Chen L, Stewart V (2008) Purine utilization by Klebsiella oxytoca M5al: genes for ring-oxidizing and -opening enzymes. J Bacteriol 191(3):1006–1017. https://doi.org/10.1128/jb.01281-08

    Article  PubMed  PubMed Central  Google Scholar 

  13. Garattini E, Mendel R, Romão MJ, Wright R, Terao M (2003) Mammalian molybdo-flavoenzymes, an expanding family of proteins: structure, genetics, regulation, function and pathophysiology. Biochem J 372(1):15–32. https://doi.org/10.1042/bj20030121

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  14. Llamas A, Chamizo-Ampudia A, Tejada-Jimenez M, Galvan A, Fernandez E (2017) The molybdenum cofactor enzyme mARC: moonlighting or promiscuous enzyme? BioFactors 43(4):486–494. https://doi.org/10.1002/biof.1362

    Article  PubMed  CAS  Google Scholar 

  15. Bray R (1975) 6 Molybdenum iron-sulfur flauin hydroxylases and related enzymes. Enzymes. https://doi.org/10.1016/s1874-6047(08)60229-2

    Article  Google Scholar 

  16. Berry CE, Hare JM (2004) Xanthine oxidoreductase and cardiovascular disease: molecular mechanisms and pathophysiological implications. J Physiol 555(3):589–606. https://doi.org/10.1113/jphysiol.2003.055913

    Article  PubMed  CAS  Google Scholar 

  17. Nishino T, Okamoto K, Eger BT, Pai EF, Nishino T (2008) Mammalian xanthine oxidoreductase—mechanism of transition from xanthine dehydrogenase to xanthine oxidase. FEBS J 275(13):3278–3289. https://doi.org/10.1111/j.1742-4658.2008.06489.x

    Article  PubMed  CAS  Google Scholar 

  18. Ng’oma E, Groth M, Ripa R, Platzer M, Cellerino A (2014) Transcriptome profiling of natural dichromatism in the annual fishes Nothobranchius furzeri and Nothobranchius kadleci. BMC Genomics 15(1):754. https://doi.org/10.1186/1471-2164-15-754

    Article  PubMed  PubMed Central  Google Scholar 

  19. Zhou X, Riddiford LM (2008) rosy function is required for juvenile hormone effects in Drosophila melanogaster. Genetics 178(1):273–281. https://doi.org/10.1534/genetics.107.080754

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  20. Terao M, Romão MJ, Leimkühler S, Bolis M, Fratelli M, Coelho C, Garattini E (2016) Structure and function of mammalian aldehyde oxidases. Arch Toxicol 90(4):753–780. https://doi.org/10.1007/s00204-016-1683-1

    Article  PubMed  CAS  Google Scholar 

  21. Kurosaki M, Bolis M, Fratelli M, Barzago MM, Pattini L, Perretta G, Garattini E (2012) Structure and evolution of vertebrate aldehyde oxidases: from gene duplication to gene suppression. Cell Mol Life Sci 70(10):1807–1830. https://doi.org/10.1007/s00018-012-1229-5

    Article  PubMed  CAS  Google Scholar 

  22. Marelja Z, Dambowsky M, Bolis M, Georgiou ML, Garattini E, Missirlis F, Leimkuhler S (2014) The four aldehyde oxidases of Drosophila melanogaster have different gene expression patterns and enzyme substrate specificities. J Exp Biol 217(12):2201–2211. https://doi.org/10.1242/jeb.102129

    Article  PubMed  PubMed Central  Google Scholar 

  23. Gomezanduro G, Barillasmury C, Peregrinouriarte A, Gupta L, Gollasgalvan T, Hernandezlopez J, Yepizplascencia G (2006) The cytosolic manganese superoxide dismutase from the shrimp Litopenaeus vannamei: molecular cloning and expression. Dev Comp Immunol 30(10):893–900. https://doi.org/10.1016/j.dci.2006.01.002

    Article  CAS  Google Scholar 

  24. Muñoz M, Cedeño R, Rodríguez J, Van der Knaap WP, Mialhe E, Bachère E (2000) Measurement of reactive oxygen intermediate production in haemocytes of the penaeid shrimp, Penaeus vannamei. Aquaculture 191(1–3):89–107. https://doi.org/10.1016/s0044-8486(00)00420-8

    Article  Google Scholar 

  25. Tacon AG (2017) Biosecure shrimp feeds and feeding practices: guidelines for future development. J World Aquac Soc 48(3):381–392. https://doi.org/10.1111/jwas.12406

    Article  Google Scholar 

  26. Bulbul MG, Kader MA, Asaduzzaman M, Ambak MA, Chowdhury AJ, Hossain MS, Koshio S (2016) Can canola meal and soybean meal be used as major dietary protein sources for kuruma shrimp Marsupenaeus japonicus? Aquaculture 452:194–199. https://doi.org/10.1016/j.aquaculture.2015.10.036

    Article  CAS  Google Scholar 

  27. Thitamadee S, Prachumwat A, Srisala J, Jaroenlak P, Salachan PV, Sritunyalucksana K, Itsathitphaisarn O (2016) Review of current disease threats for cultivated penaeid shrimp in Asia. Aquaculture 452:69–87. https://doi.org/10.1016/j.aquaculture.2015.10.028

    Article  Google Scholar 

  28. García-Triana A, Peregrino-Uriarte AB, Yepiz-Plascencia G (2016) Selenoprotein M gene expression, peroxidases activity and hydrogen peroxide concentration are differentially regulated in gill and hepatopancreas of the white shrimp Litopenaeus vannamei during hypoxia and reoxygenation. Comp Biochem Physiol Part A Mol Integr Physiol 199:14–20. https://doi.org/10.1016/j.cbpa.2016.04.019

    Article  CAS  Google Scholar 

  29. Messner B, Boll M (1994) Cell suspension cultures of spruce (Picea abies): inactivation of extracellular enzymes by fungal elicitor-induced transient release of hydrogen peroxide (oxidative burst). Plant Cell Tissue Organ Cult 39(1):69–78. https://doi.org/10.1007/bf00037594

    Article  CAS  Google Scholar 

  30. Letunic I, Doerks T, Bork P (2011) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res. https://doi.org/10.1093/nar/gkr931

    Article  PubMed  PubMed Central  Google Scholar 

  31. Kobayashi K, Miki M, Okamoto K, Nishino T (1993) Electron transfer process in milk xanthine dehydrogenase as studied by pulse radiolysis. J Biol Chem 268:24642–24646

    PubMed  CAS  Google Scholar 

  32. Olson JS, Ballou DP, Palmer G, Massey V (1974) The mechanism of action of xanthine oxidase. J Biol Chem 249:4363–4382

    PubMed  CAS  Google Scholar 

  33. Kanda M, Brady FO, Rajagopalan KV, Handler P (1972) Studies on the dissociation of flavin adenine dinucleotide from metalloflavoproteins. J Biol Chem 247:765– 70

    PubMed  CAS  Google Scholar 

  34. Komai H, Massey V, Palmer G (1969) The preparation and properties of deflavo xanthine oxidase. J Biol Chem 244:1692–1700

    PubMed  CAS  Google Scholar 

  35. Harrison R (2002) Structure and function of xanthine oxidoreductase: where are we now? Free Radic Biol Med 33(6):774–797. https://doi.org/10.1016/s0891-5849(02)00956-5

    Article  PubMed  CAS  Google Scholar 

  36. Wright RM, Vaitaitis GM, Wilson CM, Repine TB, Terada LS, Repine JE (1993) cDNA cloning, characterization, and tissue-specific expression of human xanthine dehydrogenase/xanthine oxidase. Proc Natl Acad Sci USA 90(22):10690–10694. https://doi.org/10.1073/pnas.90.22.10690

    Article  PubMed  CAS  Google Scholar 

  37. Kim YS, Nam HJ, Chung HY, Kim ND, Ryu JH, Lee WJ, Yoo MA (2001) Role of xanthine dehydrogenase and aging on the innate immune response of Drosophila. J Am Aging Assoc 24(4):187–193. https://doi.org/10.1007/s11357-001-0020-6

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  38. Seymour KJ, Roberts LE, Fini MA, Parmley LA, Oustitch TL, Wright RM (2006) Stress activation of mammary epithelial cell xanthine oxidoreductase is mediated by p38 MAPK and CCAAT/enhancer-binding protein-β. J Biol Chem 281(13):8545–8558. https://doi.org/10.1074/jbc.m507349200

    Article  PubMed  CAS  Google Scholar 

  39. Zhang Y, Wang W, Li M, Li S, Liu S (2017) Identification of putative carboxylesterase and aldehyde oxidase genes from the antennae of the rice leaffolder, Cnaphalocrocis medinalis (Lepidoptera: Pyralidae). J Asia Pac Entomol 20(3):907–913. https://doi.org/10.1016/j.aspen.2017.06.001

    Article  Google Scholar 

  40. Pongsomboon S, Wongpanya R, Tang S, Chalorsrikul A, Tassanakajon A (2008) Abundantly expressed transcripts in the lymphoid organ of the black tiger shrimp, Penaeus monodon, and their implication in immune function. Fish Shellfish Immunol 25(5):485–493. https://doi.org/10.1016/j.fsi.2008.07.010

    Article  PubMed  CAS  Google Scholar 

  41. Kamli MR, Kim J, Pokharel S, Jan AT, Lee EJ, Choi I (2014) Expressional studies of the aldehyde oxidase (AOX1) gene during myogenic differentiation in C2C12 cells. Biochem Biophys Res Commun 450(4):1291–1296. https://doi.org/10.1016/j.bbrc.2014.06.126

    Article  PubMed  CAS  Google Scholar 

  42. Kundu TK, Hille R, Velayutham M, Zweier JL (2007) Characterization of superoxide production from aldehyde oxidase: an important source of oxidants in biological tissues. Arch Biochem Biophys 460(1):113–121. https://doi.org/10.1016/j.abb.2006.12.032

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  43. Yergaliyev TM, Nurbekova Z, Mukiyanova G, Akbassova A, Sutula M, Zhangazin S, Omarov RT (2016) The involvement of ROS producing aldehyde oxidase in plant response to Tombusvirus infection. Plant Physiol Biochem 109:36–44. https://doi.org/10.1016/j.plaphy.2016.09.001

    Article  PubMed  CAS  Google Scholar 

  44. Inada M, Kihara K, Kono T, Sudhakaran R, Mekata T, Sakai M, Itami T (2013) Deciphering of the dual oxidase (Nox family) gene from kuruma shrimp, Marsupenaeus japonicus: full-length cDNA cloning and characterization. Fish Shellfish Immunol 34(2):471–485. https://doi.org/10.1016/j.fsi.2012.11.026

    Article  PubMed  CAS  Google Scholar 

  45. Blokhina O (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91(2):179–194. https://doi.org/10.1093/aob/mcf118

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  46. Arbi M, Pouliliou S, Lampropoulou M, Marmaras VJ, Tsakas S (2011) Hydrogen peroxide is produced by E. coli challenged haemocytes and regulates phagocytosis, in the medfly Ceratitis capitata. The active role of superoxide dismutase. Dev Comp Immunol 35(8):865–871. https://doi.org/10.1016/j.dci.2011.03.020

    Article  PubMed  CAS  Google Scholar 

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Acknowledgements

This work was supported by JSPS-KAKENHI a Grant-in-Aid for Scientific Research (C) 15K07555 and Grant- in-Aid for Young Scientists (B) 16K18747. We would like to thank Editage (http://www.editage.jp) for English language editing.

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Correspondence to Toshiaki Itami.

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Research involving human participants and/or animals

The kuruma shrimp that our target species in this study is edible shrimp in Japan. So, this study is not applicable study in this item. However, before dissecting, the kuruma shrimp was immersed into the iced water for around 5 mm into fall into suspended animation.

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Okamura, Y., Inada, M., Elshopakey, G.E. et al. Characterization of xanthine dehydrogenase and aldehyde oxidase of Marsupenaeus japonicus and their response to microbial pathogen. Mol Biol Rep 45, 419–432 (2018). https://doi.org/10.1007/s11033-018-4177-9

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