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Transcript profiles of mitochondrial and cytoplasmic manganese superoxide dismutases in Exopalaemon carinicauda under ammonia stress

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Abstract

Superoxide dismutase (SOD) is one of the most important antioxidant defense enzymes, and is considered as the first line against oxidative stress. In this study, we cloned a mitochondrial manganese (Mn) SOD (mMnSOD) cDNA from the ridgetail white prawn Exopalaemon carinicauda by using rapid amplification of cDNA ends (RACE) methods. The full-length cDNA for mMnSOD was 1 014-bp long, containing a 5′-untranslated region (UTR) of 37-bp, a 3′-UTR of 321-bp with a poly (A) tail, and included a 657-bp open reading frame encoding a protein of 218 amino acids with a 16-amino-acid signal peptide. The protein had a calculated molecular weight of 23.87 kDa and a theoretical isoelectric point of 6.75. The mMnSOD sequence included two putative N-glycosylation sites (NHT and NLS), the MnSOD signature sequence 180DVWEHAYY187, and four putative Mn binding sites (H48, H96, D180, and H184). Sequence comparison showed that the mMnSOD deduced amino acid sequence of E. carinicauda shared 97%, 95%, 89%, 84%, 82%, 72%, and 69% identity with that of Macrobrachium rosenbergii, Macrobrachium nipponense, Fenneropeneaus chinensis, Callinectes sapidus, Perisesarma bidens, Danio rerio, and Homo sapiens, resectively. Quantitative real-time RT-PCR analysis showed that mMnSOD transcripts were present in all E. carinicauda tissues examined, with the highest levels in the hepatopancreas. During an ammonia stress treatment, the transcript levels of mMnSOD and cMnSOD were up-regulated at 12 h in hemocytes and at 24 h in the hepatopancreas. As the duration of the ammonia stress treatment extended to 72 h, the transcript levels of mMnSOD and cMnSOD significantly decreased both in hemocytes and hepatopancreas. These findings indicate that the SOD system is induced to respond to acute ammonia stress, and may be involved in environmental stress responses in E. carinicauda.

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References

  • Areekit S, Kanjanavas P, Khawsak P, Pakpitchareon A, Potivejkul K, Chansiri G, Chansiri k. 2011. Cloning, expression, and characterization of thermotolerant manganese superoxide dismutase from Bacillus sp. MHS47. International Journal of Molecular Sciences, 12(1): 844–856, http://dx.doi.org/10.3390/ijms12010844.

    Article  Google Scholar 

  • Brouwer M, Hoexum Brouwer T, Grater W, Brown-Peterson N. 2003. Replacement of a cytosolic copper/zinc superoxide dismutase by a novel cytosolic manganese superoxide dismutase in crustaceans that use copper (haemocyanin) for oxygen transport. Biochemical Journal, 374(Pt 1): 219–228, http://dx.doi.org/10.1042/BJ20030272.

    Article  Google Scholar 

  • Chandra J, Samali A, Orrenius S. 2000. Triggering and modulation of apoptosis by oxidative stress. Free Radical Biology and Medicine, 29(3–4): 323–333, http://dx.doi.org/10.1016/S0891-5849(00)00302-6.

    Article  Google Scholar 

  • Chen J C, Liu P C, Lei S C. 1990. Toxicity of ammonia and nitrite to Penaeus monodon adolescents. Aquaculture, 89(2): 127–137, http://dx.doi.org/10.1016/0044-8486(90)90305-7.

    Article  Google Scholar 

  • Chen Y Y, Sim S S, Chiew S L, Yeh S T, Liou C H, Chen J C. 2012. Dietary administration of a Gracilaria tenuistipitata extract produces protective immunity of white shrimp Litopenaeus vannamei in response to ammonia stress. Aquaculture, 370–371: 26–31, http://dx.doi.org/10.1016/j.aquaculture.2012.09.031.

    Article  Google Scholar 

  • Cheng W, Tung Y H, Chiou T T, Chen J C. 2006. Cloning and characterisation of mitochondrial manganese superoxide dismutase (mtMnSOD) from the giant freshwater prawn Macrobrachium rosenbergii. Fish & Shellfish Immunology, 21(4): 453–466, http://dx.doi.org/10.1016/j.fsi.2006.02.005.

    Article  Google Scholar 

  • Cheng W T, Tung Y H, Liu C H, Chen J C. 2006. Molecular cloning and characterisation of cytosolic manganese superoxide dismutase (cytMn-SOD) from the giant freshwater prawn Macrobrachium rosenbergii. Fish & Shellfish Immunology, 20(4): 438–449, http://dx.doi.org/10.1016/j.fsi.2005.05.016.

    Article  Google Scholar 

  • Duan Y F, Liu P, Li J T, Li J, Chen P. 2013. Expression profiles of selenium dependent glutathione peroxidase and glutathione S-transferase from Exopalaemon carinicauda in response to Vibrio anguillarum and WSSV challenge. Fish & Shellfish Immunology, 35(3): 661–670, http://dx.doi.org/10.1016/j.fsi.2013.05.016.

    Article  Google Scholar 

  • Fridovich I. 1975. Superoxide dismutases. Annual Review of Biochemistry, 44: 147–159, http://dx.doi.org/10.1146/annurev.bi.44.070175.001051.

    Article  Google Scholar 

  • Fridovich I. 1995. Superoxide radical and superoxide dismutases. Annual Review of Biochemistry, 64: 97–112, http://dx.doi.org/10.1146/annurev.bi.64.070195.000525.

    Article  Google Scholar 

  • García-Triana A, Zenteno-Savín T, Peregrino-Uriarte AB, Yepiz-Plascencia G. 2010. Hypoxia, reoxygenation and cytosolic manganese superoxide dismutase (cMnSOD) silencing in Litopenaeus vannamei: effects on cMnSOD transcripts, superoxide dismutase activity and superoxide anion production capacity. Developmental & Comparative Immunology, 34(11): 1 230–1 235, http://dx.doi.org/10.1016/j.dci.2010.06.018.

    Article  Google Scholar 

  • Gómez-Anduro G A, Barillas-Mury C V, Peregrino-Uriarte A B, Gupta L, Gollas-Galván T, Hernández-López J, Yepiz-Plascenciaa G. 2006. The cytosolic manganese superoxide dismutase from the white shrimp Litopenaeus vannamei: molecular cloning and expression. Developmental & Comparative Immunology, 30(10): 893–900, http://dx.doi.org/10.1016/j.dci.2006.01.002.

    Article  Google Scholar 

  • González-Rodríguez G, Colubi A, Gil M A. 2012. Fuzzy data treated as functional data: a one-way ANOVA test approach. Computational Statistics & Data Analysis, 56(4): 943–955, http://dx.doi.org/10.1016/j.csda.2010.06.013.

    Article  Google Scholar 

  • Huang X H, Li C L, Liu C W, Zheng L, He J. 2002. Studies on two microalgae improving environment of shrimp pond and strengthening anti-disease ability of Penaeus vannamei. Acta Hydrobiologica Sinica, 26(4): 342–347. (in Chinese with English abstract)

    Google Scholar 

  • Jo P G, Choi Y K, Choi C Y. 2008. Cloning and mRNA expression of antioxidant enzymes in the Pacific oyster, Crassostrea gigas in response to cadmium exposure. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 147(4): 460–469, http://dx.doi.org/10.1016/j.cbpc.2008.02.001.

    Google Scholar 

  • Li J T, Chen P, Liu P, Gao B Q, Wang Q Y, Li J. 2010. The cytosolic manganese superoxide dismutase cDNA in swimming crab Portunus trituberculatus: molecular cloning, characterization and expression. Aquaculture, 309(1–4): 31–37, http://dx.doi.org/10.1016/j.aquaculture.2010.09.008.

    Article  Google Scholar 

  • Lightner DV, Redman R M. 1998, Shrimp disease and current diagnostic methods. Aquaculture, 164(1–4): 201–220, http://dx.doi.org/10.1016/S0044-8486(98)00187-2.

    Article  Google Scholar 

  • Lin Y C, Lee F F, Wu C L, Chen J C. 2010. Molecular cloning and characterization of a cytosolic manganese superoxide dismutase (cytMnSOD) and mitochondrial manganese superoxide dismutase (mtMnSOD) from the kuruma shrimp Marsupenaeus japonicus. Fish & Shellfish Immunology, 28(1): 143–150, http://dx.doi.org/10.1016/j.fsi.2009.10.012.

    Article  Google Scholar 

  • Liu C H, Chen J C. 2004. Effect of ammonia on the immune response of white shrimp Litopenaeus vannamei and its susceptibility to Vibrio alginolyticus. Fish & Shellfish Immunology, 16(3): 321–334, http://dx.doi.org/10.1016/S1050-4648(03)00113-X.

    Article  Google Scholar 

  • Maltby L. 1995. Sensitivity of the crustaceans Gammarus pulex (L.) and Astllus aquaticus (L.) to short-term exposure to hyposia and unionized ammonia: observations and possible mechanism. Water Res earch, 29(3): 781–787, http://dx.doi.org/10.1016/0043-1354(94)00231-U.

    Article  Google Scholar 

  • Marchand J, Leignel V, Moreau B, Chénais B. 2009. Characterization and sequence analysis of manganese superoxide dismutases from Brachyura (Crustacea: Decapoda): hydrothermal Bythograeidae versus littoral crabs. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology, 153(2): 191–199, http://dx.doi.org/10.1016/j.cbpb.2009.02.019.

    Article  Google Scholar 

  • Meng Q G, Chen J, Xu C C, Huang Y Q, Wang Y, Wang T T, Zhai X T, Gu W, Wang W. 2013. The characterization, expression and activity analysis of superoxide dismutases (SODs) from Procambarus clarki i. Aquaculture, 406–407: 131–140, http://dx.doi.org/10.1016/j.aquaculture.2013.05.008.

    Article  Google Scholar 

  • Nimptsch J. Pflugmacher S. 2007. Ammonia triggers the promotion of oxidative stress in the aquatic macrophyte, Myriophyllum mattogrossense. Chemosphere, 66(4): 708–714, http://dx.doi.org/10.1016/j.chemosphere.2006.07.064.

    Article  Google Scholar 

  • Pan C H, Chien Y H, Hunter B. 2003. The resistance to ammonia stress of Penaeus monodon Fabricius juvenile fed diets supplemented with astaxanthin. Journal of Experimental Marine Biology and Ecology, 297(1): 107–118, http://dx.doi.org/10.1016/j.jembe.2003.07.002.

    Article  Google Scholar 

  • Park H, Ahn I Y, Lee J K, Shin S C, Lee J, Choy E J. 2009. Molecular cloning, characterization, and the response of manganese superoxide dismutase from the Antarctic bivalve Laternula elliptica to PCB exposure. Fish & Shellfish Immunology, 27(3): 522–528, http://dx.doi.org/10.1016/j.fsi.2009.07.008.

    Article  Google Scholar 

  • Pipe R K, Porte C, Livingstone D R. 1993. Antioxidant enzymes associated with the blood cells and haemolymph of the mussel Mytilus edulis. Fish & Shellfish Immunology, 3(3): 221–333, http://dx.doi.org/10.1006/fsim.1993.1022.

    Article  Google Scholar 

  • Randall D J, Tsui T K N. 2002. Ammonia toxicity in fish. Marine Pollution Bulletin, 45(1–12): 17–23, http://dx.doi.org/10.1016/S0025-326X(02)00227-8.

    Article  Google Scholar 

  • Ren H, Li J, Li J T, Liang Z X, Liang J P, Ge Q Q, Liu P. 2014. Effects of acute ammonia stresses on antioxidant system enzyme activities and GPx gene expression in Exopalaemon carinicauda. Journal of Agro-Environment Science, 33(4): 647–655. (in Chinese with English abstract)

    Google Scholar 

  • Shen H, Wan X H, Wang L B, Fei R M, Li S, Bai L, Ling Y, Li H, Gao B. 2013. Study on experimental infection of Exopalaemon carinicauda Holehuis with white spot syndrome virus. Marine Sciences, 37(5): 55–60. (in Chinese with English abstract)

    Google Scholar 

  • Sook Chung J, Bachvaroff T, Trant J, Place A. 2012. A second copper zinc superoxide dismutase (CuZnSOD) in the blue crab Callinectes sapidus: cloning and up-regulated expression in the hemocytes after immune challenge. Fish & Shellfish Immunology, 32(1): 16–25, http://dx.doi.org/10.1016/j.fsi.2011.08.023.

    Article  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA 4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution, 24(8): 1 596–1 599, http://dx.doi.org/10.1093/molbev/msm092.

    Article  Google Scholar 

  • Tang T, Huang D W, Zhou C Q, Li X, Xie Q J, Liu F S. 2012, Molecular cloning and expression patterns of copper/zinc superoxide dismutase and manganese superoxide dismutase in Musca domestica. Gene, 505(2): 211–220, http://dx.doi.org/10.1016/j.gene.2012.06.025.

    Article  Google Scholar 

  • Wang W N, Zhou J, Wang P, Tian T T, Zheng Y, Liu Y, Mai W J, Wang A L. 2009. Oxidative stress, DNA damage and antioxidant enzyme gene expression in the Pacific white shrimp Litopenaeus vannamei when exposed to acute pH stress. Comparative Biochemistry and Physiology Part C: Toxicology & Pharmacology, 150(4): 428–435, http://dx.doi.org/10.1016/j.cbpc.2009.06.010.

    Google Scholar 

  • Xu D D, Liu X H, Cao J M Du Z Y, Huang Y H, Zhao H X, Xie C X. 2012. Dietary glutathione as an antioxidant improves resistance to ammonia exposure in Litopenaeus vannamei. Aquaculture Research, 43(2): 311–316, http://dx.doi.org/10.1111/j.1365-2109.2011.02820.x.

    Article  Google Scholar 

  • Xu W J, Xie J J, Shi H, Li C W. 2010. Hematodinium infections in cultured ridgetail white prawns, Exopalaemon carinicauda, in eastern China. Aquaculture, 300(1): 25–31, http://dx.doi.org/10.1016/j.aquaculture.2009.12.024.

    Article  Google Scholar 

  • Zeng Y Y, Jiang Y X, Ai C X. 2011. Effects of ammonia-N stress on the activities of superoxide dismutase and glutathione peroxidase in different tissues and organs of Scylla paramamosain. Journal of Oceanography in Taiwan Strait, 30(2): 210–215. (in Chinese with English abstract)

    Google Scholar 

  • Zhang J F, Wang X R, Guo H Y, Wu J C, Xue Y Q. 2004. Effects of water-soluble fractions of diesel oil on the antioxidant defenses of the goldfish, Carassius auratus. Ecotoxicology and Environmental Safety, 58(1): 110–116, http://dx.doi.org/10.1016/j.ecoenv.2003.08.025.

    Article  Google Scholar 

  • Zhang Q L, Li F H, Wang B, Zhang J Q, Liu Y C, Zhou Q, Xiang J H. 2007. The mitochondrial manganese superoxide dismutase gene in Chinese shrimp Fenneropenaeus chinensis: cloning, distribution and expression. Developmental & Comparative Immunology, 31(5): 429–440, http://dx.doi.org/10.1016/j.dci.2006.08.005.

    Article  Google Scholar 

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Authors and Affiliations

  1. Hebei Normal University of Science and Technology, Qinhuangdao, 066004, China

    Hai Ren  (任海) & Jianhua Wu  (吴建华)

  2. Key Laboratory of Sustainable Development of Marine Fisheries, Ministry of Agriculture, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, 266071, China

    Hai Ren  (任海), Jian Li  (李健), Jitao Li  (李吉涛), Ping Liu  (刘萍) & Zhongxiu Liang  (梁忠秀)

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  1. Hai Ren  (任海)
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  2. Jian Li  (李健)
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Correspondence to Jian Li  (李健).

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Supported by the National High Technology Research and Development Program of China (863 Program) (No. 2012AA10A409), the Modern Agro-Industry Technology Research System (No. CARS-47), the Special Fund for Independent Innovation of Shandong Province (No. 2013CX80202), and the Special Fund for Agro-Scientific Research in the Public Interest (No. 201103034)

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Ren, H., Li, J., Li, J. et al. Transcript profiles of mitochondrial and cytoplasmic manganese superoxide dismutases in Exopalaemon carinicauda under ammonia stress. Chin. J. Ocean. Limnol. 33, 714–724 (2015). https://doi.org/10.1007/s00343-015-4143-5

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