Selectively Enhanced Expression of Prophenoloxidase Activating Enzyme 1 (PPAE1) at a Bacteria Clearance Site in the White Shrimp, Litopenaeus Vannamei

Overview

Journal BMC Immunol

Publisher Biomed Central

Specialty Allergy & Immunology

Date 2012 Jan 3

PMID 22208405

Citations 5

Authors

In-Kwon Jang

Zhenguo Pang

Jiaping Yu

Su-Kyoung Kim

Hyung-Cheol Seo

Yeong-Rok Cho

Affiliations

Soon will be listed here.

Abstract

Background: The prophenoloxidase-activating (PO activating) system plays an important role in the crustacean innate immunity, particularly in wound healing and pathogen defense. A key member of this system is prophenoloxidase-activating enzyme (PPAE), which is the direct activator of prophenoloxidase (proPO). Despite their importance in crustacean PO activating system, the studies on them remain limited.

Results: Here we report on a PPAE of white shrimp, Litopenaeus vannamei (lvPPAE1), which showed 94% similarity to PPAE1 of Penaeus monodon. We found that lvPPAE1 in fluid hemocytes was down regulated after challenge by Vibrio harveyi but was enhanced when shrimps were exposed to a bacteria-rich environment for long-term. In vivo gene silence of lvPPAE1 by RNAi can significantly reduce the phenoloxidase activity (PO) and increase the susceptibility of shrimps to V. harveyi. Although lvPPAE1 was down-regulated in fluid hemocytes by Vibrio challenge, its expression increased significantly in gill after bacteria injection, which is the primary bacteria-clearance tissue.

Conclusion: Suppressed expression in fluid hemocytes and enhanced expression in gill indicates selectively enhanced expression at the bacterial clearance site. This is a novel feature for PPAE expression. The results will contribute to our understanding of the PO activating system in crustaceans.

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References

Cerenius L, Soderhall K . The prophenoloxidase-activating system in invertebrates. Immunol Rev. 2004; 198:116-26. DOI: 10.1111/j.0105-2896.2004.00116.x. View

Lemaitre B, Hoffmann J . The host defense of Drosophila melanogaster. Annu Rev Immunol. 2007; 25:697-743. DOI: 10.1146/annurev.immunol.25.022106.141615. View

Iwanaga S, Lee B . Recent advances in the innate immunity of invertebrate animals. J Biochem Mol Biol. 2005; 38(2):128-50. DOI: 10.5483/bmbrep.2005.38.2.128. View

Charoensapsri W, Amparyup P, Hirono I, Aoki T, Tassanakajon A . Gene silencing of a prophenoloxidase activating enzyme in the shrimp, Penaeus monodon, increases susceptibility to Vibrio harveyi infection. Dev Comp Immunol. 2009; 33(7):811-20. DOI: 10.1016/j.dci.2009.01.006. View

Ai H, Liao J, Huang X, Yin Z, Weng S, Zhao Z . A novel prophenoloxidase 2 exists in shrimp hemocytes. Dev Comp Immunol. 2008; 33(1):59-68. DOI: 10.1016/j.dci.2008.07.017. View

Charoensapsri W, Amparyup P, Hirono I, Aoki T, Tassanakajon A . PmPPAE2, a new class of crustacean prophenoloxidase (proPO)-activating enzyme and its role in PO activation. Dev Comp Immunol. 2010; 35(1):115-24. DOI: 10.1016/j.dci.2010.09.002. View

Jiravanichpaisal P, Lee B, Soderhall K . Cell-mediated immunity in arthropods: hematopoiesis, coagulation, melanization and opsonization. Immunobiology. 2006; 211(4):213-36. DOI: 10.1016/j.imbio.2005.10.015. View

Wang Y, Jiang H . Reconstitution of a branch of the Manduca sexta prophenoloxidase activation cascade in vitro: snake-like hemolymph proteinase 21 (HP21) cleaved by HP14 activates prophenoloxidase-activating proteinase-2 precursor. Insect Biochem Mol Biol. 2007; 37(10):1015-25. PMC: 2077082. DOI: 10.1016/j.ibmb.2007.05.013. View

Sritunyalucksana K, Cerenius L, Soderhall K . Molecular cloning and characterization of prophenoloxidase in the black tiger shrimp, Penaeus monodon. Dev Comp Immunol. 1999; 23(3):179-86. DOI: 10.1016/s0145-305x(99)00005-1. View

10.

Aspan A, Huang T, Cerenius L, Soderhall K . cDNA cloning of prophenoloxidase from the freshwater crayfish Pacifastacus leniusculus and its activation. Proc Natl Acad Sci U S A. 1995; 92(4):939-43. PMC: 42612. DOI: 10.1073/pnas.92.4.939. View

11.

Ai H, Huang Y, Li S, Weng S, Yu X, He J . Characterization of a prophenoloxidase from hemocytes of the shrimp Litopenaeus vannamei that is down-regulated by white spot syndrome virus. Fish Shellfish Immunol. 2008; 25(1-2):28-39. DOI: 10.1016/j.fsi.2007.12.002. View

12.

Liu H, Jiravanichpaisal P, Cerenius L, Lee B, Soderhall I, Soderhall K . Phenoloxidase is an important component of the defense against Aeromonas hydrophila Infection in a crustacean, Pacifastacus leniusculus. J Biol Chem. 2007; 282(46):33593-33598. DOI: 10.1074/jbc.M706113200. View

13.

De Gregorio E, Spellman P, Rubin G, Lemaitre B . Genome-wide analysis of the Drosophila immune response by using oligonucleotide microarrays. Proc Natl Acad Sci U S A. 2001; 98(22):12590-5. PMC: 60098. DOI: 10.1073/pnas.221458698. View

14.

Wang Y, Zou Z, Jiang H . An expansion of the dual clip-domain serine proteinase family in Manduca sexta: gene organization, expression, and evolution of prophenoloxidase-activating proteinase-2, hemolymph proteinase 12, and other related proteinases. Genomics. 2005; 87(3):399-409. PMC: 2071929. DOI: 10.1016/j.ygeno.2005.10.003. View

15.

Cerenius L, Lee B, Soderhall K . The proPO-system: pros and cons for its role in invertebrate immunity. Trends Immunol. 2008; 29(6):263-71. DOI: 10.1016/j.it.2008.02.009. View

16.

Fujimoto K, Masuda K, Asada N, Ohnishi E . Purification and characterization of prophenoloxidases from pupae of Drosophila melanogaster. J Biochem. 1993; 113(3):285-91. DOI: 10.1093/oxfordjournals.jbchem.a124040. View

17.

Wang R, Lee S, Cerenius L, Soderhall K . Properties of the prophenoloxidase activating enzyme of the freshwater crayfish, Pacifastacus leniusculus. Eur J Biochem. 2001; 268(4):895-902. DOI: 10.1046/j.1432-1327.2001.01945.x. View

18.

Asano T, Ashida M . Cuticular pro-phenoloxidase of the silkworm, Bombyx mori. Purification and demonstration of its transport from hemolymph. J Biol Chem. 2000; 276(14):11100-12. DOI: 10.1074/jbc.M008426200. View

19.

Bao Y, Yamano Y, Morishima I . Beta-1,3-glucan inducible expression of prophenoloxidase-activating proteinase from eri-silkworm, Samia cynthia ricini. Comp Biochem Physiol B Biochem Mol Biol. 2007; 147(1):45-8. DOI: 10.1016/j.cbpb.2006.12.016. View

20.

Zou Z, Wang Y, Jiang H . Manduca sexta prophenoloxidase activating proteinase-1 (PAP-1) gene: organization, expression, and regulation by immune and hormonal signals. Insect Biochem Mol Biol. 2005; 35(6):627-36. PMC: 2020815. DOI: 10.1016/j.ibmb.2005.02.004. View