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Investigation on oxidative stress of nitric oxide synthase interacting protein from Clonorchis sinensis

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Abstract

Numerous evidences indicate that excretory–secretory products (ESPs) from liver flukes trigger the generation of free radicals that are associated with the initial pathophysiological responses in host cells. In this study, we first constructed a Clonorchis sinensis (C. sinensis, Cs)-infected BALB/c mouse model and examined relative results respectively at 3, 5, 7, and 9 weeks postinfection (p.i.). Quantitative reverse transcription (RT)-PCR indicated that the transcriptional level of both endothelial nitric oxide synthase (eNOS) and superoxide dismutase (SOD) gradually decreased with lastingness of infection, while the transcriptional level of inducible NOS (iNOS) significantly increased. The level of malondialdehyde (MDA) in sera of infected mouse significantly increased versus the healthy control group. These results showed that the liver of C. sinensis-infected mouse was in a state with elevated levels of oxidation stress. Previously, C. sinensis NOS interacting protein coding gene (named CsNOSIP) has been isolated and recombinant CsNOSIP (rCsNOSIP) has been expressed in Escherichia coli, which has been confirmed to be a component present in CsESPs and confirmed to play important roles in immune regulation of the host. In the present paper, we investigated the effects of rCsNOSIP on the lipopolysaccharide (LPS)-induced activated RAW264.7, a murine macrophage cell line. We found that endotoxin-free rCsNOSIP significantly promoted the levels of nitric oxide (NO) and reactive oxygen species (ROS) after pretreated with rCsNOSIP, while the level of SOD decreased. Furthermore, rCsNOSIP could also increase the level of lipid peroxidation MDA. Taken together, these results suggested that CsNOSIP was a key molecule which was involved in the production of nitric oxide (NO) and its reactive intermediates, and played an important role in oxidative stress during C. sinensis infection.

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References

  • Bae Y-A, Ahn D-W, Lee E-G, Kim S-H, Cai G-B et al (2013) Differential activation of diverse glutathione transferases of Clonorchis sinensis in response to the host bile and oxidative stressors. PLoS Negl Trop Dis 7(5), e2211

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bateman RM, Sharpe MD, Ellis CG (2003) Bench-to-bedside review: microvascular dysfunction in sepsis-hemodynamics, oxygen transport, and nitric oxide. Crit Care 7:359–373

    Article  PubMed  PubMed Central  Google Scholar 

  • Bian M, Li S, Wang X, Xu Y, Chen W, Zhou C, Chen X, He L, Xu J, Liang C, Wu Z, Huang Y, Li X, Yu X (2014) Identification, immunolocalization, and immunological characterization of nitric oxide synthase interacting protein from Clonorchis sinensis. Parasitol Res 113(5):1749–1757

    Article  PubMed  Google Scholar 

  • Bouvard V, Baan R, Straif K, Grosse Y, Secretan B et al (2009) A review of human carcinogens-Part B: biological agents. Lancet Oncol 10:321–322

    Article  PubMed  Google Scholar 

  • Bredt DS, Snyder SH (1994) Nitric oxide: a physiologic messenger molecule. Annu RevBiochem 63:175–195

    Article  CAS  Google Scholar 

  • Curtin JF, Donovan M, Cotter TG (2002) Regulation and measurement of oxidative stress in apoptosis. J Immunol Methods 265:49–72

    Article  CAS  PubMed  Google Scholar 

  • Droge W (2002) Free radicals in the physiological control of cell function. Physiol Rev 82:47–95

    Article  CAS  PubMed  Google Scholar 

  • Halliwell B (2006) Phagocyte-derived reactive species: salvation or suicide? Trends Biochem Sci 31:509–515

    Article  CAS  PubMed  Google Scholar 

  • Huang Y, Li W, Huang L, Hu F, Chen W, Wang X, Sun J, Liang C, Wu Z, Li X, Xu J, Yu X (2012) Identification and characterization of myophilin-like protein: a life stage and tissue-specific antigen of Clonorchis sinensis. Parasitol Res 111:1143–1150

    Article  PubMed  Google Scholar 

  • Kawanishi S, Hiraku Y, Pinlaor S et al (2006) Oxidative and nitrative DNA damage in animals and patients with inflammatory diseases in relation to inflammation-related carcinogenesis. Biol Chem 387:365–372

    Article  CAS  PubMed  Google Scholar 

  • König P, Dedio J, Oess S, Papadakis T, Fischer A, Müller-Esterl W, Kummer W (2005) NOSIP and its interacting protein, eNOS, in the rat trachea and lung. J Histochem Cytochem 53(2):155–164

    Article  PubMed  Google Scholar 

  • Laothong U, Pinlaor P, Hiraku Y, Boonsiri P, Prakobwong S, Khoontawad J, Pinlaor S (2010) Protective effect of melatonin against Opisthorchis viverrini-induced oxidative and nitrosative DNA damage and liver injury in hamsters. J. Pineal Res 49:271–282

    Article  CAS  Google Scholar 

  • Lun ZR, Gasser RB, Lai DH, Li AX, Zhu XQ, Yu XB, Fang YY (2005) Clonorchiasis: a key foodborne zoonosis in China. Lancet Infect Dis 5(1):31–41

    Article  PubMed  Google Scholar 

  • Lv X, Chen W, Wang X, Li X, Sun J, Deng C, Men J, Tian Y, Zhou C, Lei H, Liang C, Yu X (2011) Molecular characterization and expression of a cysteine protease from Clonorchis sinensis and its application for serodiagnosis of clonorchiasis. Parasitol Res 110:2211–2219

    Article  PubMed  Google Scholar 

  • Nam JH, Moon JH, Kim IK, Lee MR, Hong SJ, Ahn JH, Chung JW, Pak JH (2012) Free radicals enzymatically triggered by Clonorchis sinensis excretory-secretory products cause NF-kB-mediated inflammation in human cholangiocarcinoma cells. Int J Parasitol 42:103–113

    Article  CAS  PubMed  Google Scholar 

  • Nahrevanian H (2009) Involvement of nitric oxide and its up/down stream molecules in the immunity against parasitic infections. Braz J Infect Dis 13(6):440–448

    CAS  PubMed  Google Scholar 

  • Ohshima H, Sawa T, Akaike T (2006) 8-Nitroguanine, a product of nitrative DNA damage caused by reactive nitrogen species: formation, occurrence, and implications in inflammation and carcinogenesis. Antioxid Redox Signal 8:1033–1045

    Article  CAS  PubMed  Google Scholar 

  • Pak JH, Moon JH, Hwang SJ, Cho SH, Seo SB, Kim TS (2009) Proteomic analysis of differentially expressed proteins in human cholangiocarcinoma cells treated with Clonorchis sinensis excretory-secretory products. J Cell Biochem 108:1376–1388

    Article  CAS  PubMed  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29(9), e45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pinlaor S, Hiraku Y, Ma N, Yongvanit P, Semba R (2004) Mechanism of NO-mediated oxidative and nitrative DNA damage in hamsters infected with Opisthorchis viverrini: a model of inflammation mediated carcinogenesis. Nitric Oxide 11:175–183

    Article  CAS  PubMed  Google Scholar 

  • Pinlaor S, Yongvanit P, Hiraku Y, Ma N, Semba R (2003) 8-nitroguanine formation in the liver of hamsters infected with Opisthorchis viverrini. Biochem Biophys Res Commun 309:567–571

    Article  CAS  PubMed  Google Scholar 

  • Rim HJ (2005) Clonorchiasis: an update. J Helminthol 79:269–281

    Article  PubMed  Google Scholar 

  • Serradell MC, Guasconi L, Masih DT (2009) Involvement of mitochondrial pathway and key role of hydrogen peroxide during eosinophil apoptosis induced by excretory-secretory products from Faciola hepatica. Mol Biochem Parasitol 163:95–106

    Article  CAS  PubMed  Google Scholar 

  • Thannickal VJ, Fanburg BL (2000) Reactive oxygen species in cell signaling. Am J Physiol Lung Cell Mol Physiol 279:L1005–L1028

    CAS  PubMed  Google Scholar 

  • Vennervald BJ, Polman K (2009) Helminths and malignancy. Parasite Immunol 31:686–696

    Article  CAS  PubMed  Google Scholar 

  • Wang X, ChenW LX, Tian Y, Men J, Zhang X, Lei H, Zhou C, Lu F, Liang C, Hu X, Xu J, Wu Z, Li X, Yu X (2012) Identification and characterization of paramyosin from cyst wall of metacercariae implicated protective efficacy against Clonorchis sinensis infection. PLoS ONE 7(3), e33703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoon BI, Choi YK, Kim DY, Hyun BH, Joo KH, Rim HJ, Lee JY (2001) Infectivity and pathological changes in murine clonorchiasis: comparison in immnocompetent and immunodefective mice. J Vet Med Sci 63:421–425

    Article  CAS  PubMed  Google Scholar 

  • Young ND, Campbell BE, Hall RS, Jex AR, Cantacessi C, Laha T, Sohn WM, Sripa B, Loukas A, Brindley PJ, Gasser RB (2010) Unlocking the transcriptomes of two carcinogenic parasites, Clonorchis sinensis and Opisthorchis viverrini. PLoS Negl Trop Dis 4(6), e719

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhou C, Bian M, Liao H, Mao Q, Li R, Zhou J, Wang X, Li S, Liang C, Li X, Huang Y, Yu X (2013) Identification and immunological characterization of thioredoxin transmembrane-related protein from Clonorchis sinensis. Parasitol Res 112(4):1729–36

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by grants from the Guangdong Natural Science Foundation of China (No. 2014A030313027), the National Important Sci-tech Special Projects (No. 2012ZX10004220), the National Key Basic Research and Development Project of China (973 project; No.2010CB530000), and the National Natural Science Foundation of China (No. 82201270 and No. 81171602).

Competing interests

The authors declare that they have no competing interests.

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    Authors and Affiliations

    1. Department of Clinical Laboratory, Affiliated Tumor Hospital of Zhengzhou University, Henan Tumor Hospital, Zhengzhou, Henan, China

      Meng Bian, Qingxia Xu & Jiahe Sheng

    2. Key Laboratory for Tropical Diseases Control, Ministry of Education, Sun Yat-sen University, Guangzhou, 510080, People’s Republic of China

      Meng Bian, Yanquan Xu, Shan Li, Xiaoyun Wang, Zhongdao Wu, Yan Huang & Xinbing Yu

    3. Department of Pathology and Pathophysiology, Henan University of Traditional Chinese Medicine, Zhengzhou, 450000, People’s Republic of China

      Shan Li

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    1. Meng Bian
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    Correspondence to Xinbing Yu.

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    Meng Bian and Qingxia Xu contributed equally to this work.

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    Bian, M., Xu, Q., Xu, Y. et al. Investigation on oxidative stress of nitric oxide synthase interacting protein from Clonorchis sinensis . Parasitol Res 115, 77–83 (2016). https://doi.org/10.1007/s00436-015-4723-5

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