Skip to main content

Advertisement

SpringerLink
Log in

Inflammatory Injury and Mitophagy in the Cock Heart Induced by the Oral Administration of Hexavalent Chromium

  • Published:
Biological Trace Element Research Aims and scope Submit manuscript

Abstract

As a highly toxic heavy metal, chromium has caused a certain threat to public health and livestock breeding in recent years. In poultry, as one of our most commonly consumed meat product, its health issues will seriously threaten the safety of human life. As previous studies have confirmed, when cells are stimulated by the external environment, mitochondria, as an organelle that provides energy to the cells, can cause damage and autophagy. The purpose of this study is to confirm whether Cr(VI) can cause mitophagy in cock heart. We first randomly divided 32 cocks into four groups to explore the mechanism of this effect. The cocks were then separately exposed to four different dose levels, namely, the control level and 10, 30, and 50 mg/kg levels, via daily oral intake into the body through mixed feeding for 45 days. After 45 days, we sampled and detected pathological changes and the levels of inflammatory factors (IL-6, TNF-α, and IFN-γ), mitochondrial membrane potential (MMP), adenosine triphosphatases (ATPases), and mitophagy-related proteins (LC3, p62/SQTM1, TOMM20, and Parkin). We found that IL-6, TNF-α, IFN-γ, and LC3II contents increased with the increase in Cr(VI) concentration. However, MMP, ATPases, p62/SQTM1, and TOMM20 levels decreased with the increase in Cr(VI) concentration. At the same time, Cr(VI) exposure caused heart tissue damages and Parkin translocation. In conclusion, our results proved that inflammatory damage, mitochondrial function damage, and mitophagy in cock heart tissues were dependent on Cr(VI) concentration.

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

Similar content being viewed by others

References

  1. Beaver LM, Stemmy EJ, Constant SL, Schwartz A, Little LG, Gigley JP, Chun G, Sugden KD, Ceryak SM, Patierno SR (2009) Lung injury, inflammation and Akt signaling following inhalation of particulate hexavalent chromium. Toxicol Appl Pharmacol 235:47–56

    Article  CAS  Google Scholar 

  2. Boeri M, Oliveri C, Camurati C, Viarengo A, Sforzini S (2017) Effects of Cr(VI) on Ca(2+)-ATPase activity in the earthworm Eisenia andrei. Comp Biochem Physiol C Toxicol Pharmacol 203:21–28

    Article  CAS  Google Scholar 

  3. Boşgelmez I, Güvendik G (2017) N-Acetyl-L-cysteine protects liver and kidney against chromium(VI)-induced oxidative stress in mice. Biol Trace Elem Res 178:44–53

    Article  Google Scholar 

  4. Boşgelmez I, Güvendik G (2019) Beneficial effects of N-Acetyl-L-cysteine or taurine pre- or post-treatments in the heart, spleen, lung, and testis of hexavalent chromium-exposed mice. Biol Trace Elem Res 190:437–445

    Article  Google Scholar 

  5. Chen P, Geng N, Zhou D, Zhu Y, Xu Y, Liu K, Liu Y, Liu J (2019) The regulatory role of COX-2 in the interaction between Cr(VI)-induced endoplasmic reticulum stress and autophagy in DF-1 cells. Ecotoxicol Environ Saf 170:112–119

    Article  CAS  Google Scholar 

  6. Collins BJ, Stout MD, Levine KE, Kissling GE, Melnick RL, Fennell TR, Walden R, Abdo K, Pritchard JB, Fernando RA, Burka LT, Hooth MJ (2010) Exposure to hexavalent chromium resulted in significantly higher tissue chromium burden compared with trivalent chromium following similar oral doses to male F344/N rats and female B6C3F1 mice. Toxicol Sci 118:368–379

    Article  CAS  Google Scholar 

  7. DesMarais TL, Costa M (2019) Mechanisms of chromium-induced toxicity. Curr Opin Toxicol 14:1–7

    Article  Google Scholar 

  8. Fan WT, Zhao XN, Cheng J, Liu YH, Liu JZ (2015) Oxidative stress and hepatocellular injury induced by oral administration of Cr(3+) in chicken. J Biochem Mol Toxicol 29:280–287

    Article  CAS  Google Scholar 

  9. García-Niño WR, Zatarain-Barrón ZL, Hernández-Pando R, Vega-García CC, Tapia E, Pedraza-Chaverri J (2015) Oxidative stress markers and histological analysis in diverse organs from rats treated with a hepatotoxic dose of Cr(VI): effect of curcumin. Biol Trace Elem Res 167:130–145

    Article  Google Scholar 

  10. Hao J, Song Y, Tian B, Qi C, Li L, Wang L, Xing Y, Zhao X, Liu J (2020) Platycodon grandifloras polysaccharides inhibit mitophagy injury induced by Cr (VI) in DF-1 cells. Ecotoxicol Environ Saf 202:110901

    Article  CAS  Google Scholar 

  11. Hao P, Zhu Y, Wang S, Wan H, Chen P, Wang Y, Cheng Z, Liu Y, Liu J (2017) Selenium administration alleviates toxicity of chromium(VI) in the chicken brain. Biol Trace Elem Res 178:127–135

    Article  CAS  Google Scholar 

  12. He L, Zhou Q, Huang Z, Xu J, Zhou H, Lv D, Lu L, Huang S, Tang M, Zhong J, Chen JX, Luo X, Li L, Chen L (2019) PINK1/Parkin-mediated mitophagy promotes apelin-13-induced vascular smooth muscle cell proliferation by AMPKα and exacerbates atherosclerotic lesions. J Cell Physiol 234:8668–8682

    Article  CAS  Google Scholar 

  13. Karlstad J et al (2012) Ca(2+) signaling: an outlook on the characterization of Ca(2+) channels and their importance in cellular functions. Adv Exp Med Biol 740:143–157

    Article  CAS  Google Scholar 

  14. Khan ZI, Ahmad K, Siddique S, Ahmad T, Bashir H, Munir M, Mahpara S, Malik IS, Wajid K, Ugulu I, Nadeem M, Noorka IR, Chen F (2020) A study on the transfer of chromium from meadows to grazing livestock: an assessment of health risk. Environ Sci Pollut Res Int 27:26694–26701

    Article  CAS  Google Scholar 

  15. Kim I, Rodriguez-Enriquez S, Lemasters JJ (2007) Selective degradation of mitochondria by mitophagy. Arch Biochem Biophys 462:245–253

    Article  CAS  Google Scholar 

  16. Li J, Zheng X, Ma X, Xu X, du Y, Lv Q, Li X, Wu Y, Sun H, Yu L, Zhang Z (2019) Melatonin protects against chromium(VI)-induced cardiac injury via activating the AMPK/Nrf2 pathway. J Inorg Biochem 197:110698

    Article  CAS  Google Scholar 

  17. Lin J, Zhao HS, Xiang LR, Xia J, Wang LL, Li XN, Li JL, Zhang Y (2016) Lycopene protects against atrazine-induced hepatic ionic homeostasis disturbance by modulating ion-transporting ATPases. J Nutr Biochem 27:249–256

    Article  CAS  Google Scholar 

  18. Liu K, Chen P, Lu J, Zhu Y, Xu Y, Liu Y, Liu J (2020) Protective effect of purple tomato anthocyanidin on chromium(VI)-induced autophagy in LMH cells by inhibiting endoplasmic reticulum stress. Biol Trace Elem Res 194:570–580

    Article  CAS  Google Scholar 

  19. Liu Y, Liu C, Cheng J, Fan W, Zhang X, Liu J (2015) Growth performance and oxidative damage in kidney induced by oral administration of Cr(III) in chicken. Chemosphere. 139:365–371

    Article  CAS  Google Scholar 

  20. Lu J, Liu K, Qi M, Geng H, Hao JJ, Wang R, Zhao X, Liu Y, Liu J (2019) Effects of Cr(VI) exposure on electrocardiogram, myocardial enzyme parameters, inflammatory factors, oxidative kinase, and ATPase of the heart in Chinese rural dogs. Environ Sci Pollut Res Int 26:30444–30451

    Article  CAS  Google Scholar 

  21. Mishra S, Bharagava RN (2016) Toxic and genotoxic effects of hexavalent chromium in environment and its bioremediation strategies. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 34:1–32

    Article  CAS  Google Scholar 

  22. Moretto A (2015) Hexavalent and trivalent chromium in leather: What should be done? Regul Toxicol Pharmacol 73:681–686

    Article  CAS  Google Scholar 

  23. Nguyen TN, Padman BS, Lazarou M (2016) Deciphering the molecular signals of PINK1/parkin mitophagy. Trends Cell Biol 26:733–744

    Article  CAS  Google Scholar 

  24. Rahman Z, Singh VP (2019) The relative impact of toxic heavy metals (THMs) (arsenic (As), cadmium (Cd), chromium (Cr)(VI), mercury (Hg), and lead (Pb)) on the total environment: an overview. Environ Monit Assess 191:419

    Article  Google Scholar 

  25. Rovira-Llopis S, Bañuls C, Diaz-Morales N, Hernandez-Mijares A, Rocha M, Victor VM (2017) Mitochondrial dynamics in type 2 diabetes: pathophysiological implications. Redox Biol 11:637–645

    Article  CAS  Google Scholar 

  26. Salama A, Hegazy R, Hassan A (2016) Intranasal chromium induces acute brain and lung injuries in rats: assessment of different potential hazardous effects of environmental and occupational exposure to chromium and introduction of a novel pharmacological and toxicological animal model. PLoS One 11:e0168688

    Article  Google Scholar 

  27. Sauvé V, Sung G, Soya N, Kozlov G, Blaimschein N, Miotto LS, Trempe JF, Lukacs GL, Gehring K (2018) Mechanism of parkin activation by phosphorylation. Nat Struct Mol Biol 25:623–630

    Article  Google Scholar 

  28. Suljevic D et al (2021) Assessing hexavalent chromium tissue-specific accumulation patterns and induced physiological responses to probe chromium toxicity in Coturnix japonica quail. Chemosphere. 266:129005

    Article  CAS  Google Scholar 

  29. Suzuki K, Ohsumi Y (2007) Molecular machinery of autophagosome formation in yeast, Saccharomyces cerevisiae. FEBS Lett 581:2156–2161

    Article  CAS  Google Scholar 

  30. Tziakas D, Chalikias G, Parissis JT, Hatzinikolaou H, Stakos D, Papadopoulou E, Kortsaris A, Hatseras D (2004) Prolonged activation of tumor necrosis factor (TNF)-alpha and its soluble receptors in chronic heart failure patients both in the compensated and decompensated state. Interplay between their levels and metalloproteinase-3. Eur Cytokine Netw 15:231–239

    CAS  PubMed  Google Scholar 

  31. Wan H, Zhu Y, Chen P, Wang Y, Hao P, Cheng Z, Liu Y, Liu J (2017) Effect of various selenium doses on chromium(IV)-induced nephrotoxicity in a male chicken model. Chemosphere. 174:306–314

    Article  CAS  Google Scholar 

  32. Wang Y, Hao J, Zhang S, Li L, Wang R, Zhu Y, Liu Y, Liu J (2020) Inflammatory injury and mitophagy induced by Cr(VI) in chicken liver. Environ Sci Pollut Res Int 27:22980–22988

    Article  CAS  Google Scholar 

  33. Wedeen RP, Qian LF (1991) Chromium-induced kidney disease. Environ Health Perspect 92:71–74

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Xu Y, Wang X, Geng N, Zhu Y, Zhang S, Liu Y, Liu J (2020) Mitophagy is involved in chromium (VI)-induced mitochondria damage in DF-1 cells. Ecotoxicol Environ Saf 194:110414

    Article  CAS  Google Scholar 

  35. Yamada T, Dawson TM, Yanagawa T, Iijima M, Sesaki H (2019) SQSTM1/p62 promotes mitochondrial ubiquitination independently of PINK1 and PRKN/parkin in mitophagy. Autophagy. 15:2012–2018

    Article  CAS  Google Scholar 

  36. Yang CP et al (2019) Olanzapine induced dysmetabolic changes involving tissue chromium mobilization in female rats. Int J Mol Sci 20(3):640

  37. Yatera K et al (2018) Cancer risks of hexavalent chromium in the respiratory tract. J UOEH 40:157–172

    Article  CAS  Google Scholar 

  38. Yin J, Wang AP, Li WF, Shi R, Jin HT, Wei JF (2018) Time-response characteristic and potential biomarker identification of heavy metal induced toxicity in zebrafish. Fish Shellfish Immunol 72:309–317

    Article  CAS  Google Scholar 

  39. Zhang Y, Bian H, Ma Y, Xiao Y, Xiao F (2020) Cr(VI)-induced overactive mitophagy contributes to mitochondrial loss and cytotoxicity in L02 hepatocytes. Biochem J 477:2607–2619

    Article  CAS  Google Scholar 

  40. Zhu Y, Xu G, Chen P, Liu K, Xu Y, Liu Y, Liu J (2019) Effects of Cr(VI)-induced calcium-sensing receptor activation on DF-1 cell pyroptosis. Ecotoxicol Environ Saf 179:257–264

    Article  CAS  Google Scholar 

Download references

Funding

This project was supported by the National Nature Science Foundation of China (No. 31872535, 31802259), Shandong Natural Science Foundation of China (ZR2018MC027), Shandong Key R&D Program (GG201809160113), China Postdoctoral Science Foundation (2018M632704, 2019T120601), and Funds of Shandong “Double Tops” Program.

Author information

Author notes

  1. Yue Wang and Lumei Wang contributed equally to this work.

Authors and Affiliations

  1. College of Veterinary Medicine, China Agricultural University, Beijing, 100193, People’s Republic of China

    Yue Wang

  2. College of Veterinary Medicine, Shandong Agricultural University, Tai’an, 271018, Shandong, China

    Lumei Wang, Xiaozhou Wang, Guodong Cheng, Yuxiao Xing, Meihua Zhang & Jianzhu Liu

  3. Central Hospital of Tai’an City, Tai’an, 271018, Shandong, China

    Pu Zhang

Authors
  1. Yue Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Lumei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiaozhou Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Guodong Cheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Yuxiao Xing
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Meihua Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Pu Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Jianzhu Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Pu Zhang or Jianzhu Liu.

Ethics declarations

Conflict of Interest

The authors declare no competing interest.

Additional information

Publisher’s Note

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

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, Y., Wang, L., Wang, X. et al. Inflammatory Injury and Mitophagy in the Cock Heart Induced by the Oral Administration of Hexavalent Chromium. Biol Trace Elem Res 200, 1312–1320 (2022). https://doi.org/10.1007/s12011-021-02715-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-021-02715-0

Keywords

Search

Navigation