Cite this paper:
REN Hai, LI Jian, LI Jitao, LIU Ping, LIANG Zhongxiu, WU Jianhua. Transcript profiles of mitochondrial and cytoplasmic manganese superoxide dismutases in Exopalaemon carinicauda under ammonia stress[J]. HaiyangYuHuZhao, 2015, 33(3): 714-724

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

REN Hai1,2, LI Jian2, LI Jitao2, LIU Ping2, LIANG Zhongxiu2, WU Jianhua1
1 Hebei Normal University of Science and Technology, Qinhuangdao 066004, China;
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
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 m MnSOD 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, M acrobrachium 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.
Key words:    Exopalaemon carinicauda|mitochondrial manganese superoxide dismutase (mMnSOD)|cytosolic manganese superoxide dismutase (cMnSOD)|cloning|expression   
Received: 2014-05-07   Revised: 2014-09-06
Tools
PDF (858 KB) Free
Print this page
Add to favorites
Email this article to others
Authors
Articles by REN Hai
Articles by LI Jian
Articles by LI Jitao
Articles by LIU Ping
Articles by LIANG Zhongxiu
Articles by WU Jianhua
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.
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. Biochem ical J ournal, 374 (Pt 1): 219-228, http://dx.doi.org/10.1042/BJ20030272.
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.
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.
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.
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.
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.
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.
Fridovich I. 1975. Superoxide dismutases. Annual Review of Biochemistry, 44 : 147-159, http://dx.doi.org/10.1146/ annurev.bi.44.070175.001051.
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.
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.
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.
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.
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)
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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)
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)
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.
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.
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.
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.
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.
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.
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)
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.
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.