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In vivo and in vitro studies using Clonorchis sinensis adult-derived total protein (CsTP) on cellular function and inflammatory effect in mouse and cell model

  • Immunology and Host-Parasite Interactions - Original Paper
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Abstract

Clonorchis sinensis (C. sinensis) can induce a food-borne parasitic disease (clonorchiasis). Numerous studies have analyzed functional proteins, immunologic factors, pro-inflammatory cytokines, and cell signaling transduction that promote the development of clonorchiasis. In a previous study, it was shown that C. sinensis adult-derived total protein (CsTP) might be involved in the pathogenesis and development of liver fibrosis via bringing about Th2 immune response. In the present study, further investigation of CsTP on cellular function and inflammatory effect in vitro and in vivo has been elicited. CsTP induced inflammation and autophagy as evidenced by upregulation of TNF-α, IFN-γ, and autophagic markers LC3B and P62. Exposed to CsTP upregulated the antiapoptotic gene Bcl-2 expression, diminished the apoptosis induced by H2O2, but promoted the proliferation and migration of LX-2 cells in proper concentration range. Additionally, the protein levels of p-AKT and p-mTOR were repressed in response to CsTP, suggesting a correlation of blocking the activation of mTOR/AKT signaling pathway. These results revealed that CsTP might exacerbate hepatic pathological changes by regulating cell proliferation, apoptosis, autophagy, and inflammation in the liver and LX-2 cells. Some effects might be partially involved in the mTOR and AKT pathways.

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Abbreviations

CsTP:

Clonorchis sinensis adult-derived total protein

ESPs:

excretory-secretory products

s.c:

subcutaneously

FBS:

fetal bovine serum

ELISA:

enzyme-linked immunosorbent assay

DAPI:

4′, 6-Diamidino-2-Phenylindole

TNF-α:

tumor necrosis factor-alpha

IFN-γ:

Interferon-gamma

DCs:

dendritic cell

TI-TP:

total protein of the adult worm Toxascaris leonina

OVA:

ovalbumin

PBMC:

peripheral blood mononuclear cells

SWA:

Schistosoma mansoni adult worm antigen

Sh:

S. haematobium total antigens

CHO:

Chinese hamster ovary

VEGF:

vascular endothelial growth factor

NAG:

N-acetyl-β-D-glucosaminidase

scFv:

B cell single-chain antibody Fv

LC3B:

microtubule-associated proteins 1A/1B light chain 3B

GAPDH:

glyceraldehyde 3-phosphate dehydrogenase

Bcl-2:

B cell lymphoma 2

p-mTOR:

phospho-mTOR

IL-1β:

interleukin-1β

HRP:

horseradish peroxidase

CCK-8:

cell count kit-8

HBV:

hepatitis B virus

HSC:

hepatic stellate cell

KCs:

Kuffer cells

DHA:

dihydroartemisinin

RA-FLS:

rheumatoid arthritis fibroblast-like synoviocytes

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Acknowledgments

We appreciate Ph.D Danika Bakke, Ph.D Zhiyu Dai, and Ph.D Xiaoyun Wang for helping to improve the writing of this final manuscript.

Availability of data and materials

The datasets generated and/or analyzed during the current study are available in the Clonorchis sinensis Genome Database repository, [http://fluke.sysu.edu.cn/CsinGD/].

Funding

This work was supported by grants from Guangdong Natural Science Foundation (No. 2019A1515010583), the National Natural Science Foundation of China (No. 81641094), National Key Research and Development Program of China (Nos. 2016YFC1202003, 2016YFC1202005), and Guangdong Natural Science Foundation (No. 2019A1515010583, S2012010008504) to XL. The national key research and development program of China (No. 2017YFD0501300), Guangdong marine economy promotion projects fund (GDOE[2019]A29), and the science and technology planning project of Guangdong province (No. 2014B020203001) to XY. The National Natural Science Foundation of China (Nos. 81,101,270, 31,372,263) to YH and YW, respectively.

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Author notes

  1. Mei Shang and Hengchang Sun contributed equally to this work.

Authors and Affiliations

  1. Department of Clinical Laboratory, The Third Affiliated Hospital of Sun Yat-sen University, Guangzhou, 510630, People’s Republic of China

    Mei Shang & Hengchang Sun

  2. Department of Parasitology, Zhongshan School of Medicine, Sun Yat-sen University, Guangzhou, 510080, People’s Republic of China

    Mei Shang, Hengchang Sun, Yinjuan Wu, Zeli Tang, Lei He, Xinbing Yu, Yan Huang & Xuerong Li

  3. Key Laboratory for Tropical Disease Control, Sun Yat-sen University, Guangzhou, 510080, People’s Republic of China

    Mei Shang, Hengchang Sun, Yinjuan Wu, Zeli Tang, Lei He, Xinbing Yu, Yan Huang & Xuerong Li

  4. Department of Endoscopy, National Cancer Center/National Clinical Research Center for Cancer/Cancer Hospital, Chinese Academy of Medical Sciences and Peking Union Medical College, Beijing, 100021, People’s Republic of China

    Yu Gong

  5. Department of Cell Biology and Genetics, School of Pre-clinical Medicine, Guangxi Medical University, Nanning, 530021, People’s Republic of China

    Zeli Tang

  6. Department of Joint Surgery, First Affiliated Hospital of Sun Yat-sen University, Guangzhou, 510080, China

    Fangang Meng

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  1. Mei Shang
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Correspondence to Yan Huang or Xuerong Li.

Ethics declarations

All Balb/c mice used in the study were purchased from Animal Center of Sun Yat-sen University and raised with caution based on animal care and the ethical guidelines of the National Institutes of Health. The operation of whole animal studies was approved by the Sun Yat-sen University Institutional Animal Care and Use Committee (Permit Numbers: SYXK (Guangdong) 2010–0107).

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Shang, M., Sun, H., Wu, Y. et al. In vivo and in vitro studies using Clonorchis sinensis adult-derived total protein (CsTP) on cellular function and inflammatory effect in mouse and cell model. Parasitol Res 119, 1641–1652 (2020). https://doi.org/10.1007/s00436-020-06651-1

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