Skip to main content
SpringerLink
Log in

Curcumin antagonizes inflammation and autophagy induced by arsenic trioxide through immune protection in duck spleen

  • Research Article
  • Published:
Environmental Science and Pollution Research Aims and scope Submit manuscript

Abstract

Arsenic is a toxic heavy metal widely found in the natural environment and has adverse effects on the health of waterfowl and human. Curcumin (CUR), a natural pigment of the golden spice turmeric, exhibits excellent anti-tumor, anti-inflammatory and anti-oxidant activities. But the effects of CUR on duck spleen exposed to arsenic remain largely unknown. In this study, 75 ducks were divided randomly into Control, L-ATO, M-ATO, H-ATO and CUR + H-ATO groups to systematically analyze the underlying role of CUR. The results showed that arsenic trioxide (ATO) led to growth retardation of ducks, hyaline degeneration and sparse cell arrangement on their spleen. And in the ATO-exposed ducks, the levels of immunoglobulins (Ig; IgA, IgG, IgM) in the serum and the expression of autophagy-related genes (Atg5, P62, LC3I, LC3II, LC3II/I, Beclin-1) were significantly upregulated compared with the control ducks. Moreover, ATO also activated NF-κB signal pathway and upregulated the expression of pro-inflammatory cytokines (TNF-α, IFN-γ, IL-1β, IL-2, IL-18). Meanwhile, application of CUR alleviated the ATO toxicity with the release of growth inhibition, and the reduced hyaline degeneration and distortion of the spleen capsule. CUR also suppressed ATO-induced NF-κB activation, pro-inflammatory cytokine addition and expression of autophagy-related genes. Overall, these results suggested that CUR might exert a protective effect against ATO-induced immunosuppression in ducks via anti-inflammation and autophagy restoring.

Graphical abstract

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  • Abdel-Daim MM, Abo-El-Sooud K et al (2018) Alleviation of drugs and chemicals toxicity: biomedical value of antioxidants. Oxid Med Cell Longev 2018:6276438

    Google Scholar 

  • Bahrami A, Sathyapalan T et al (2020a) Counteracting arsenic toxicity: curcumin to the rescue? J Hazard Mater 400:123160

    Article  CAS  Google Scholar 

  • Bahrami A, Sathyapalan T et al (2020b) Counteracting arsenic toxicity: curcumin to the rescue? J Hazard Mater 400:123160

    CAS  Google Scholar 

  • Burge K, Gunasekaran A et al (2019) Curcumin and intestinal inflammatory diseases: molecular mechanisms of protection. Int J Mol Sci 20(8)

  • Choudhury S, Ghosh S et al (2016) Pomegranate protects against arsenic-induced p53-dependent ROS-mediated inflammation and apoptosis in liver cells. J Nutr Biochem 38:25–40

    CAS  Google Scholar 

  • Cordero H, Morcillo P et al (2018) Inorganic arsenic causes apoptosis cell death and immunotoxicity on European sea bass (Dicentrarchus labrax). Mar Pollut Bull 128:324–332

    CAS  Google Scholar 

  • Deretic V, Saitoh T et al (2013) Autophagy in infection, inflammation and immunity. Nat Rev Immunol 13(10):722–737

    CAS  Google Scholar 

  • Duan X, Gao S et al (2017) Acute arsenic exposure induces inflammatory responses and CD4(+) T cell subpopulations differentiation in spleen and thymus with the involvement of MAPK, NF-kB, and Nrf2. Mol Immunol 81:160–172

    CAS  Google Scholar 

  • Fang Y, Xing C et al (2021) Activation of the ROS/HO-1/NQO1 signaling pathway contributes to the copper-induced oxidative stress and autophagy in duck renal tubular epithelial cells. Sci Total Environ 757:143753

    CAS  Google Scholar 

  • Gelfand EW (2012) Intravenous immune globulin in autoimmune and inflammatory diseases. N Engl J Med 367(21):2015–2025

    CAS  Google Scholar 

  • Hull EA, Barajas M et al (2021) Human health risk from consumption of aquatic species in arsenic-contaminated shallow urban lakes. Sci Total Environ 770:145318

    CAS  Google Scholar 

  • Jamal Z, Das J et al (2020) Arsenic-induced immunomodulatory effects disorient the survival-death interface by stabilizing the Hsp90/Beclin1 interaction. Chemosphere 238:124647

    CAS  Google Scholar 

  • Jiang X, Yu W et al (2021) Arsenic (III) and/or Antimony (III) induced disruption of calcium homeostasis and endoplasmic reticulum stress resulting in apoptosis in mice heart. Ecotoxicol Environ Saf 220:112394

    CAS  Google Scholar 

  • Kim JH, Kang JC (2016) The immune responses and expression of metallothionein (MT) gene and heat shock protein 70 (HSP 70) in juvenile rockfish, Sebastes schlegelii, exposed to waterborne arsenic (As(3+)). Environ Toxicol Pharmacol 47:136–141

    CAS  Google Scholar 

  • Levine B, Mizushima N et al (2011a) Autophagy in immunity and inflammation. Nature 469(7330):323–335

    CAS  Google Scholar 

  • Levine B, Mizushima N et al (2011b) Autophagy in immunity and inflammation. Nature 469(7330):323–335

    CAS  Google Scholar 

  • Liu J, Zhao H et al (2018) Impacts of simultaneous exposure to arsenic (III) and copper (II) on inflammatory response, immune homeostasis, and heat shock response in chicken thymus. Int Immunopharmacol 64:60–68

    CAS  Google Scholar 

  • Liu J, Wang Y et al (2020) Arsenic (III) or/and copper (II) exposure induce immunotoxicity through trigger oxidative stress, inflammation and immune imbalance in the bursa of chicken. Ecotoxicol Environ Saf 190:110127

    CAS  Google Scholar 

  • Matucci A, Maggi E et al (2014) Mechanisms of action of Ig preparations: immunomodulatory and anti-inflammatory effects. Front Immunol 5:690

    Google Scholar 

  • Moscat J, Diaz-Meco MT (2009) p62 at the crossroads of autophagy, apoptosis, and cancer. Cell 137(6):1001–1004

    CAS  Google Scholar 

  • Osman A, ElFar A et al (2017) Immunity, antioxidant status, and performance of broiler chickens fed turmeric (Curcuma longa) rhizome powder. Alexandria J Veterinary Sci 54(2)

  • Saha S, Sadhukhan P et al (2018) Ameliorative role of genistein against age-dependent chronic arsenic toxicity in murine brains via the regulation of oxidative stress and inflammatory signaling cascades. J Nutr Biochem 55:26–40

    CAS  Google Scholar 

  • Salehi B, Stojanovic-Radic Z et al (2019) The therapeutic potential of curcumin: a review of clinical trials. Eur J Med Chem 163:527–545

    CAS  Google Scholar 

  • Sanchez-Virosta P, Espin S et al (2020) Arsenic-related oxidative stress in experimentally-dosed wild great tit nestlings. Environ Pollut 259:113813

    CAS  Google Scholar 

  • Sarkar S, Greenleaf JE et al (2012) Sustainable engineered processes to mitigate the global arsenic crisis in drinking water: challenges and progress. Annu Rev Chem Biomol Eng 3:497–517

    CAS  Google Scholar 

  • Sharma RA, Gescher AJ et al (2005) Curcumin: the story so far. Eur J Cancer 41(13):1955–1968

    CAS  Google Scholar 

  • Tabeshpour J, Banaeeyeh S et al (2019) Effects of curcumin on ion channels and pumps: a review. IUBMB Life 71(7):812–820

    CAS  Google Scholar 

  • Trujillo J, Chirino YI et al (2013) Renoprotective effect of the antioxidant curcumin: recent findings. Redox Biol 1:448–456

    CAS  Google Scholar 

  • Wang C, Nie G et al (2020a) Molybdenum and cadmium co-induce oxidative stress and apoptosis through mitochondria-mediated pathway in duck renal tubular epithelial cells. J Hazard Mater 383:121157

    CAS  Google Scholar 

  • Wang J, Zhang G et al (2020b) Determination of arsenicals in mouse tissues after simulated exposure to arsenic from rice for sixteen weeks and the effects on histopathological features. Ecotoxicol Environ Saf 200:110742

    CAS  Google Scholar 

  • Wang Y, Zhao H et al (2021) Zinc offers splenic protection through suppressing PERK/IRE1-driven apoptosis pathway in common carp (Cyprinus carpio) under arsenic stress. Ecotoxicol Environ Saf 208:111473

    CAS  Google Scholar 

  • Wei S, Qiu T et al (2020) Arsenic induces pancreatic dysfunction and ferroptosis via mitochondrial ROS-autophagy-lysosomal pathway. J Hazard Mater 384:121390

    CAS  Google Scholar 

  • Wu S, Zhong G et al (2021) Evaluation of toxic effects induced by arsenic trioxide or/and antimony on autophagy and apoptosis in testis of adult mice. Environ Sci Pollut Res Int 28(39):54647–54660

    CAS  Google Scholar 

  • Wu X, Guan R et al (2020) Comparative health risk assessment of realgar and NiuHuangJieDu tablets based on tissue arsenic levels after multiple oral administration to rats. J Ethnopharmacol 249:112370

    CAS  Google Scholar 

  • Xue L, Zhao Z et al (2020) Dietary exposure to arsenic and human health risks in western Tibet. Sci Total Environ 731:138840

    CAS  Google Scholar 

  • Yan N, Xu G et al (2020) Chronic arsenic exposure induces the time-dependent modulation of inflammation and immunosuppression in spleen. Cell Biosci 10:91

    CAS  Google Scholar 

  • Yang S, Qiang L et al (2017) NF-kappaB signaling activation induced by chloroquine requires autophagosome, p62 protein, and c-Jun N-terminal kinase (JNK) signaling and promotes tumor cell resistance. J Biol Chem 292(8):3379–3388

    CAS  Google Scholar 

  • Zhang C, Lin T et al (2021) In vivo assessment of molybdenum and cadmium co-induce nephrotoxicity via causing calcium homeostasis disorder and autophagy in ducks (Anas platyrhyncha). Ecotoxicol Environ Saf 230:113099

    Google Scholar 

  • Zhao H, Wang Y et al (2018a) Subchronic arsenism disorders mRNA expression of cytokines and immunoglobulins in the intestinal tract of the cock. Biol Trace Elem Res 182(1):111–118

    CAS  Google Scholar 

  • Zhao H, Wang Y et al (2018b) Subchronic arsenism disorders mRNA expression of cytokines and immunoglobulins in the intestinal tract of the cock. Biol Trace Elem Res 182(1):111–118

    CAS  Google Scholar 

  • Zhao Y, Su X et al (2019) Exposure of low-concentration arsenic-initiated inflammation and autophagy in rat lungs. J Biochem Mol Toxicol 33(7):e22334

    Google Scholar 

  • Zhong G, Wan F et al (2021a) Arsenic exposure induces intestinal barrier damage and consequent activation of gut-liver axis leading to inflammation and pyroptosis of liver in ducks. Sci Total Environ 788:147780

    CAS  Google Scholar 

  • Zhong G, Wan F et al (2021b) The protective role of autophagy against arsenic trioxide-induced cytotoxicity and ROS-dependent pyroptosis in NCTC-1469 cells. J Inorg Biochem 217:111396

    CAS  Google Scholar 

  • Zhong G, Wan F et al (2021c) The protective role of autophagy against arsenic trioxide-induced cytotoxicity and ROS-dependent pyroptosis in NCTC-1469 cells. J Inorg Biochem 217:111396

    CAS  Google Scholar 

  • Zhuang J, Nie G et al (2021) Inhibition of autophagy aggravates molybdenum-induced mitochondrial dysfunction by aggravating oxidative stress in duck renal tubular epithelial cells. Ecotoxicol Environ Saf 209:111771

    CAS  Google Scholar 

Download references

Availability of data and material

All relevant data and materials are available from the authors upon reasonable request.

Code availability

Not applicable.

Funding

This work was supported by the National Natural Science Foundation of China (#31402264); Guangxi Science and Technology Bureau (Gui Ke AA17204057, AA18118051); Program of Department of Natural Resources of Guangdong Province (GDNRC[2021]53); Projects of International Cooperation and Exchanges [NSFC(321611603)].

Author information

Authors and Affiliations

  1. College of Veterinary Medicine, South China Agricultural University, Guangzhou, 510642, China

    Lixuan Tang, Juan Lan, Xuanxuan Jiang, Qiling Pang, Shaofeng Wu, Fang Wan, Gaolong Zhong, Zhaoxin Tang & Lianmei Hu

  2. Guangdong Provincial Key Laboratory of Food Quality and Safety, College of Food Science, South China Agricultural University, Guangzhou, 510642, China

    Riming Huang

Authors
  1. Lixuan Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Juan Lan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xuanxuan Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Riming Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Qiling Pang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Shaofeng Wu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Fang Wan
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Gaolong Zhong
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Zhaoxin Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Lianmei Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Study design: FW, GZ, SW, XJ; experimental studies and data analysis: LT, LJ, SW, XJ; manuscript editing: LT, NZ; manuscript modification: ZT, RH, QP.

Corresponding author

Correspondence to Lianmei Hu.

Ethics declarations

Ethics approval

All animal procedures and experimental methods in this research were authorized by the Ethics Committee of South China Agricultural University. The treatment of animals in all experiments conforms to the ethical standards of experimental animals.

Consent to participate

Not applicable

Consent for publication

Not applicable

Conflict of interest

The authors declare no competing interests.

Additional information

Responsible Editor: Mohamed M. Abdel-Daim

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

ESM 1

(DOCX 14 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Tang, L., Lan, J., Jiang, X. et al. Curcumin antagonizes inflammation and autophagy induced by arsenic trioxide through immune protection in duck spleen. Environ Sci Pollut Res 29, 75344–75355 (2022). https://doi.org/10.1007/s11356-022-20691-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11356-022-20691-3

Keywords

Search

Navigation