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Journal of Immunology Research
Volume 2017, Article ID 7125084, 10 pages
https://doi.org/10.1155/2017/7125084
Research Article

Hemoglobins Likely Function as Peroxidase in Blood Clam Tegillarca granosa Hemocytes

1School of Marine Sciences, Ningbo University, Ningbo 315211, China
2Zhejiang Key Laboratory of Aquatic Germplasm Resources, Zhejiang Wanli University, Ningbo 315100, China

Correspondence should be addressed to Qinggang Xue; nc.ude.uwz@euxq and Yongbo Bao; moc.liamg@1002oabbob

Received 26 October 2016; Accepted 22 December 2016; Published 15 January 2017

Academic Editor: Yang Zhang

Copyright © 2017 Sufang Wang et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. R. Hardison, “Hemoglobins from bacteria to man: evolution of different patterns of gene expression,” The Journal of Experimental Biology, vol. 201, no. 8, pp. 1099–1117, 1998. View at Google Scholar · View at Scopus
  2. M. L. Coates, “Hemoglobin function in the vertebrates: an evolutionary model,” Journal of Molecular Evolution, vol. 6, no. 4, pp. 285–307, 1975. View at Publisher · View at Google Scholar · View at Scopus
  3. T. Kawano, R. Pinontoan, H. Hosoya, and S. Muto, “Monoamine-dependent production of reactive oxygen species catalyzed by pseudoperoxidase activity of human hemoglobin,” Bioscience, Biotechnology and Biochemistry, vol. 66, no. 6, pp. 1224–1232, 2002. View at Publisher · View at Google Scholar · View at Scopus
  4. C. E. Cooper, R. Silaghi-Dumitrescu, M. Rukengwa, A. I. Alayash, and P. W. Buehler, “Peroxidase activity of hemoglobin towards ascorbate and urate: a synergistic protective strategy against toxicity of Hemoglobin-Based Oxygen Carriers (HBOC),” Biochimica et Biophysica Acta (BBA)—Proteins and Proteomics, vol. 1784, no. 10, pp. 1415–1420, 2008. View at Publisher · View at Google Scholar · View at Scopus
  5. D. M. Minning, A. J. Gow, J. Bonavetura et al., “Ascaris haemoglobin is a nitric oxide-activated ‘deoxygenase’,” Nature, vol. 401, no. 6752, pp. 497–502, 1999. View at Publisher · View at Google Scholar · View at Scopus
  6. A. I. Alayash, “Hemoglobin-based blood substitutes: oxygen carriers, pressor agents, or oxidants?” Nature Biotechnology, vol. 17, no. 6, pp. 545–549, 1999. View at Publisher · View at Google Scholar · View at Scopus
  7. N. Jiang, N. S. Tan, B. Ho, and J. L. Ding, “Respiratory protein-generated reactive oxygen species as an antimicrobial strategy,” Nature Immunology, vol. 8, no. 10, pp. 1114–1122, 2007. View at Publisher · View at Google Scholar · View at Scopus
  8. M. Kvist, E. S. Ryabova, E. Nordlander, and L. Bülow, “An investigation of the peroxidase activity of Vitreoscilla hemoglobin,” Journal of Biological Inorganic Chemistry, vol. 12, no. 3, pp. 324–334, 2007. View at Publisher · View at Google Scholar · View at Scopus
  9. M. Katsu, K. Niizuma, H. Yoshioka, N. Okami, H. Sakata, and P. H. Chan, “Hemoglobin-induced oxidative stress contributes to matrix metalloproteinase activation and blood-brain barrier dysfunction in vivo,” Journal of Cerebral Blood Flow and Metabolism, vol. 30, no. 12, pp. 1939–1950, 2010. View at Publisher · View at Google Scholar · View at Scopus
  10. T.-M. Cheng, S. J. T. Mao, S.-T. Lai et al., “Haemoglobin-induced oxidative stress is associated with both endogenous peroxidase activity and H2O2 generation from polyunsaturated fatty acids,” Free Radical Research, vol. 45, no. 3, pp. 303–316, 2011. View at Publisher · View at Google Scholar · View at Scopus
  11. Y. Bao, Q. Wang, and Z. Lin, “Hemoglobin of the bloody clam Tegillarca granosa (Tg-HbI) is involved in the immune response against bacterial infection,” Fish and Shellfish Immunology, vol. 31, no. 4, pp. 517–523, 2011. View at Publisher · View at Google Scholar · View at Scopus
  12. Y. Bao, Q. Wang, H. Liu, and Z. Lin, “A small HSP gene of bloody clam (Tegillarca granosa) involved in the immune response against Vibrio parahaemolyticus and lipopolysaccharide,” Fish and Shellfish Immunology, vol. 30, no. 2, pp. 729–733, 2011. View at Publisher · View at Google Scholar · View at Scopus
  13. Y. B. Bao, Q. Wang, X. M. Guo, and Z. H. Lin, “Structure and immune expression analysis of hemoglobin genes from the blood clam Tegillarca granosa,” Genetics and Molecular Research, vol. 12, no. 3, pp. 3110–3123, 2013. View at Publisher · View at Google Scholar · View at Scopus
  14. S. Wang, Y. Bao, M. Shi et al., “Purification and antibacterial activity of hemoglobin from Tegillarca granosa,” Acta Oceanologica Sinica, vol. 36, no. 12, pp. 67–73, 2014 (Chinese). View at Google Scholar
  15. Y. Bao, J. Wang, C. Li, P. Li, S. Wang, and Z. Lin, “A preliminary study on the antibacterial mechanism of Tegillarca granosa hemoglobin by derived peptides and peroxidase activity,” Fish & Shellfish Immunology, vol. 51, pp. 9–16, 2016. View at Publisher · View at Google Scholar · View at Scopus
  16. H. Woude, Mechanisms of Toxic Action of the Flavonoid Quercetin and Its Phase II Metabolites, Ponsen & Looijen, 2006.
  17. J.-L. Primus, M. G. Boersma, D. Mandon et al., “The effect of iron to manganese substitution on microperoxidase 8 catalysed peroxidase and cytochrome P450 type of catalysis,” Journal of Biological Inorganic Chemistry, vol. 4, no. 3, pp. 274–283, 1999. View at Publisher · View at Google Scholar · View at Scopus
  18. B. Hendel, R. L. Sinsabaugh, and J. Marxsen, “Lignin-degrading enzymes: phenoloxidase and peroxidase,” in Methods to Study Litter Decomposition, pp. 273–277, Springer Netherlands, 2005. View at Google Scholar
  19. A. Mika, F. Buck, and S. Lüthje, “Membrane-bound class III peroxidases: identification, biochemical properties and sequence analysis of isoenzymes purified from maize (Zea mays L.) roots,” Journal of Proteomics, vol. 71, no. 4, pp. 412–424, 2008. View at Publisher · View at Google Scholar · View at Scopus
  20. S.-F. Wang, Y.-X. Si, Z.-J. Wang, S.-J. Yin, J.-M. Yang, and G.-Y. Qian, “Folding studies on muscle type of creatine kinase from Pelodiscus sinensis,” International Journal of Biological Macromolecules, vol. 50, no. 4, pp. 981–990, 2012. View at Publisher · View at Google Scholar · View at Scopus
  21. P. R. Ortiz De Montellano, “Catalytic sites of hemoprotein peroxidases,” Annual Review of Pharmacology and Toxicology, vol. 32, no. 1, pp. 89–107, 1992. View at Publisher · View at Google Scholar · View at Scopus
  22. Z.-H. Wang, Y.-W. Lin, F. I. Rosell et al., “Converting cytochrome c into a peroxidase-like metalloenzyme by molecular design,” ChemBioChem, vol. 8, no. 6, pp. 607–609, 2007. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Filizola and G. H. Loew, “Role of protein environment in horseradish peroxidase compound I formation: molecular dynamics simulations of horseradish peroxidase-HOOH complex,” Journal of the American Chemical Society, vol. 122, no. 1, pp. 18–25, 2000. View at Publisher · View at Google Scholar · View at Scopus
  24. N. C. Veitch, “Horseradish peroxidase: a modern view of a classic enzyme,” Phytochemistry, vol. 65, no. 3, pp. 249–259, 2004. View at Publisher · View at Google Scholar · View at Scopus
  25. G. I. Berglund, G. H. Carlsson, A. T. Smith, H. Szöke, A. Henriksen, and J. Hajdu, “The catalytic pathway of horseradish peroxidase at high resolution,” Nature, vol. 417, no. 6887, pp. 463–468, 2002. View at Publisher · View at Google Scholar · View at Scopus
  26. B. Xu, J. Zhao, Z. Jing, Y. Zhang, Y. Shi, and T. Fan, “Role of hemoglobin from blood clam Scapharca kagoshimensis beyond oxygen transport,” Fish and Shellfish Immunology, vol. 44, no. 1, pp. 248–256, 2015. View at Publisher · View at Google Scholar · View at Scopus
  27. K. Adachi, T. Hirata, T. Nishioka, and M. Sakaguchi, “Hemocyte components in crustaceans convert hemocyanin into a phenoloxidase-like enzyme,” Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, vol. 134, no. 1, pp. 135–141, 2003. View at Publisher · View at Google Scholar · View at Scopus
  28. H. Decker and E. Jaenicke, “Recent findings on phenoloxidase activity and antimicrobial activity of hemocyanins,” Developmental & Comparative Immunology, vol. 28, no. 7-8, pp. 673–687, 2004. View at Publisher · View at Google Scholar · View at Scopus
  29. T. Fan, Y. Zhang, L. Yang et al., “Identification and characterization of a hemocyanin-derived phenoloxidase from the crab Charybdis japonica,” Comparative Biochemistry and Physiology—B Biochemistry and Molecular Biology, vol. 152, no. 2, pp. 144–149, 2009. View at Publisher · View at Google Scholar · View at Scopus
  30. N. I. Siddiqui, G. Préaux, and C. Gielens, “Intrinsic and induced o-diphenoloxidase activity of β-hemocyanin of Helix pomatia,” Micron, vol. 35, no. 1-2, pp. 91–92, 2004. View at Publisher · View at Google Scholar · View at Scopus
  31. A. Daudi, Z. Cheng, J. A. O'Brien et al., “The apoplastic oxidative burst peroxidase in Arabidopsis is a major component of pattern-triggered immunity,” Plant Cell, vol. 24, no. 1, pp. 275–287, 2012. View at Publisher · View at Google Scholar · View at Scopus
  32. L. Almagro, L. V. Gómez Ros, S. Belchi-Navarro, R. Bru, A. Ros Barceló, and M. A. Pedreño, “Class III peroxidases in plant defence reactions,” Journal of Experimental Botany, vol. 60, no. 2, pp. 377–390, 2009. View at Publisher · View at Google Scholar · View at Scopus
  33. V. Borelli, F. Vita, S. Shankar et al., “Human eosinophil peroxidase induces surface alteration, killing, and lysis of Mycobacterium tuberculosis,” Infection and Immunity, vol. 71, no. 2, pp. 605–613, 2003. View at Publisher · View at Google Scholar · View at Scopus
  34. E. L. Thomas and T. M. Aune, “Cofactor role of iodide in peroxidase antimicrobial action against Escherichia coli,” Antimicrobial Agents and Chemotherapy, vol. 13, no. 6, pp. 1000–1005, 1978. View at Publisher · View at Google Scholar · View at Scopus
  35. J. N. de Wit and A. C. M. Van Hooydonk, “Structure, functions and applications of lactoperoxidase in natural antimicrobial systems,” Netherlands Milk and Dairy Journal, vol. 50, pp. 227–244, 1996. View at Google Scholar
  36. H. B. Dunford, “Peroxidase-catalyzed halide ion oxidation,” Redox Report, vol. 5, no. 4, pp. 169–171, 2000. View at Publisher · View at Google Scholar · View at Scopus
  37. G. Wojciechowski, L. Huang, and P. R. Ortiz De Montellano, “Autocatalytic modification of the prosthetic heme of horseradish but not lactoperoxidase by thiocyanate oxidation products. A role for heme-protein covalent cross-linking,” Journal of the American Chemical Society, vol. 127, no. 45, pp. 15871–15879, 2005. View at Publisher · View at Google Scholar · View at Scopus
  38. S. J. Klebanoff, “Myeloperoxidase: friend and foe,” Journal of Leukocyte Biology, vol. 77, no. 5, pp. 598–625, 2005. View at Publisher · View at Google Scholar · View at Scopus
  39. E. Malle, P. G. Furtmüller, W. Sattler, and C. Obinger, “Myeloperoxidase: a target for new drug development?” British Journal of Pharmacology, vol. 152, no. 6, pp. 838–854, 2007. View at Publisher · View at Google Scholar · View at Scopus
  40. Z. Zhu, L. Xu, and Z. Zhang, “structural characteristics and phagocytic and enzymatic activities of haemocytes in blood clam Tegillarca granosa,” Journal of Fisheries of China, vol. 10, pp. 1494–1502, 2011. View at Google Scholar