Skip to main content
SpringerLink
Log in

ATP5J and ATP5H Proactive Expression Correlates with Cardiomyocyte Mitochondrial Dysfunction Induced by Fluoride

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

Abstract

To investigate the effect of excessive fluoride on the mitochondrial function of cardiomyocytes, 20 healthy male mice were randomly divided into 2 groups of 10, as follows: control group (animals were provided with distilled water) and fluoride group (animals were provided with 150 mg/L F− drinking water). Ultrastructure and pathological morphological changes of myocardial tissue were observed under the transmission electron and light microscopes, respectively. The content of hydrolysis ATP enzyme was observed by ATP enzyme staining. The expression levels of ATP5J and ATP5H were measured by Western blot and quantitative real-time PCR. The morphology and ultrastructure of cardiomyocytes mitochondrial were seriously damaged by fluoride, including the following: concentration of cardiomyocytes and inflammatory infiltration, vague myofilaments, and mitochondrial ridge. The damage of mitochondrial structure was accompanied by the significant decrease in the content of ATP enzyme for ATP hydrolysis in the fluoride group. ATP5J and ATP5H expressions were significantly increased in the fluoride group. Thus, fluoride induced the mitochondrial dysfunction in cardiomyocytes by damaging the structure of mitochondrial and interfering with the synthesis of ATP. The proactive ATP5J and ATP5H expression levels were a good response to the mitochondrial dysfunction in cardiomyocytes.

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

Similar content being viewed by others

Reference

  1. Williams GS, Smith GD, Sobie EA, Jafri MS (2010) Models of cardiac excitation-contraction coupling in ventricular myocytes. Math Biosci 226(1):1–15

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Norman C, Rall JA, Tikunova SB, Davis JP (2007) Modulation of the rate of cardiac muscle contraction by troponin C constructs with various calcium binding affinities. Am J Physiol Heart Circ Physiol 293(4):H2580–H2587

    Article  CAS  PubMed  Google Scholar 

  3. Ren M, Liu Y, Zhao H, Dong S, Jiang Z, Li K, Tian J (2016) Adenosine triphosphate postconditioning is associated with better preserved global and regional cardiac function during myocardial ischemia and reperfusion: a speckle tracking imaging-based echocardiologic study. Cardiovasc Ther 34(5):343–351

    Article  CAS  PubMed  Google Scholar 

  4. Antico Arciuch VG, Elguero ME, Poderoso JJ, Carreras MC (2012) Mitochondrial regulation of cell cycle and proliferation. Antioxid Redox Signal 16(10):1150–1180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Bernardi P, Di Lisa F, Fogolari F, Lippe G (2015) From ATP to PTP and back: a dual function for the mitochondrial ATP synthase. Circ Res 116(11):1850–1862

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Beutner G, Alavian KN, Jonas EA, Porter GA Jr (2016) Erratum to: the mitochondrial permeability transition pore and ATP synthase. Handb Exp Pharmacol. doi:10.1007/164_2016_87

    Google Scholar 

  7. Nowak G, Bakajsova D (2015) Protein kinase C-α interaction with F0F1-ATPase promotes F0F1-ATPase activity and reduces energy deficits in injured renal cells. J Biol Chem 290(11):7054–7066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  8. Hornung T, Volkov OA, Zaida TM, Delannoy S, Wise JG, Vogel PD (2008) Structure of the cytosolic part of the subunit b-dimer of Escherichia coli F0F1-ATP synthase. Biophys J 94(12):5053–5064

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Rai AK, Spolaore B, Harris DA, Dabbeni-Sala F, Lippe G (2013) Ectopic F0F1 ATP synthase contains both nuclear and mitochondrially-encoded subunits. J Bioenerg Biomembr 45(6):569–579

    Article  CAS  PubMed  Google Scholar 

  10. Nesci S, Ventrella V, Trombetti F, Pirini M, Pagliarani A (2014) Thiol oxidation of mitochondrial F0-c subunits: a way to switch off antimicrobial drug targets of the mitochondrial ATP synthase. Med Hypotheses 83(2):160–165

    Article  CAS  PubMed  Google Scholar 

  11. Sawai H, Takai-Igarashi T, Tanaka H (2015) Identification of collaborative activities with oxidative phosphorylation in bipolar disorder. Bioinformation 11(4):207–216

    Article  PubMed  PubMed Central  Google Scholar 

  12. Croston TL, Shepherd DL, Thapa D, Nichols CE, Lewis SE, Dabkowski ER, Jagannathan R, Baseler WA, Hollander JM (2013) Evaluation of the cardiolipin biosynthetic pathway and its interactions in the diabetic heart. Life Sci 93(8):313–322

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Yan X, Yang X, Hao X, Ren Q, Gao J, Wang Y, Chang N, Qiu Y, Song G (2015) Sodium fluoride induces apoptosis in H9c2 cardiomyocytes by altering mitochondrial membrane potential and intracellular ROS level. Biol Trace Elem Res 166(2):210–215

    Article  CAS  PubMed  Google Scholar 

  14. Shim MY, Parr C, Pesti GM (2011) The effects of dietary fluoride on growth and bone mineralization in broiler chicks. Poult Sci 90(9):1967–1974

    Article  CAS  PubMed  Google Scholar 

  15. Zhou BH, Zhao J, Liu J, Zhang JL, Li J, Wang HW (2015) Fluoride-induced oxidative stress is involved in the morphological damage and dysfunction of liver in female mice. Chemosphere 139:504–511

    Article  CAS  PubMed  Google Scholar 

  16. Wang HW, Zhou BH, Cao JW, Zhao J, Zhao WP, Tan PP (2017a) Pro-inflammatory cytokines are involved in fluoride-induced cytotoxic potential in HeLa cells. Biol Trace Elem Res 175(1):98–102

    Article  CAS  PubMed  Google Scholar 

  17. Wu Z, Tang X (2015) Visualizing fluoride ion in mitochondria and lysosome of living cells and in living mice with positively charged ratiometric probes. Anal Chem 87(17):8613–8617

    Article  CAS  PubMed  Google Scholar 

  18. Wang HW, Zhao WP, Tan PP, Liu J, Zhao J, Zhou BH (2017b) The MMP-9/TIMP-1 system is involved in fluoride-induced reproductive dysfunctions in female mice. Biol Trace Elem Res. doi:10.1007/s12011-016-0929-3

    Google Scholar 

  19. El-Hattab AW, Scaglia F (2016) Mitochondrial cardiomyopathies. Front Cardiovasc Med 3:25

    Article  PubMed  PubMed Central  Google Scholar 

  20. Cicek E, Aydin G, Akdogan M, Okutan H (2005) Effects of chronic ingestion of sodium fluoride on myocardium in a second generation of rats. Hum Exp Toxicol 24(2):79–87

    Article  CAS  PubMed  Google Scholar 

  21. Liang S, Zhao MH, Ock SA, Kim NH, Cui XS (2016) Fluoride impairs oocyte maturation and subsequent embryonic development in mice. Environ Toxicol 31(11):1486–1495

    Article  CAS  PubMed  Google Scholar 

  22. Guth L, Samaha FJ (1970) Procedure for the histochemical demonstration of actomyosin ATPase. Exp Neurol 28(2):365–367

    Article  CAS  PubMed  Google Scholar 

  23. Gollnick PD, Parsons D, Oakley CR (1983) Differentiation of fiber types in skeletal muscle from the sequential inactivation of myofibrillar actomyosin ATPase during acid preincubation. Histochemistry 77(4):543–555

    Article  CAS  PubMed  Google Scholar 

  24. Dimitriu-Leen AC, Scholte AJ, Katsanos S, Hoogslag GE, van Rosendael AR, van Zwet EW, Bax JJ, Delgado V (2017) Influence of myocardial ischemia extent on left ventricular global longitudinal strain in patients after ST-segment elevation myocardial infarction. Am J Cardiol 119(1):1–6

    Article  PubMed  Google Scholar 

  25. Panneerselvam L, Govindarajan V, Ameeramja J, Nair HR, Perumal E (2015) Single oral acute fluoride exposure causes changes in cardiac expression of oxidant and antioxidant enzymes, apoptotic and necrotic markers in male rats. Biochimie 119:27–35

    Article  CAS  PubMed  Google Scholar 

  26. Panneerselvam L, Raghunath A, Perumal E (2017) Acute fluoride poisoning alters myocardial cytoskeletal and AMPK signaling proteins in rats. Int J Cardiol 229:96–101

    Article  PubMed  Google Scholar 

  27. Qin SL, Deng J, Lou DD, Yu WF, Pei J, Guan ZZ (2015) The decreased expression of mitofusin-1 and increased fission-1 together with alterations in mitochondrial morphology in the kidney of rats with chronic fluorosis may involve elevated oxidative stress. J Trace Elem Med Biol 29:263–268

    Article  CAS  PubMed  Google Scholar 

  28. Sarkar C, Pal S, Das N, Dinda B (2014) Ameliorative effects of oleanolic acid on fluoride induced metabolic and oxidative dysfunctions in rat brain: experimental and biochemical studies. Food Chem Toxicol 66:224–236

    Article  CAS  PubMed  Google Scholar 

  29. Nabavi SM, Nabavi SF, Eslami S, Moghaddam AH (2012) In vivo protective effects of quercetin against sodium fluoride-induced oxidative stress in the hepatic tissue. Food Chem 132(2):931–935

    Article  CAS  Google Scholar 

  30. Starkov AA (2008) The role of mitochondria in reactive oxygen species metabolism and signaling. Ann N Y Acad Sci 1147:37–52

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Sun ZL, Zhang W, Xue XC, Zhang YL, Niu RY, Li XY, Li BJ, Wang XW, Wang JD (2016) Fluoride decreased the sperm ATP of mice through inhabiting mitochondrial respiration. Chemosphere 144:1012–1017

    Article  CAS  PubMed  Google Scholar 

  32. Wagner K, Rehling P, Sanjuán Szklarz LK, Taylor RD, Pfanner N, van der Laan M (2009) Mitochondrial F1Fo-ATP synthase: the small subunits e and g associate with monomeric complexes to trigger dimerization. J Mol Biol 392(4):855–861

    Article  CAS  PubMed  Google Scholar 

  33. Rühle T, Leister D (2015) Assembly of F1F0-ATP synthases. Biochim Biophys Acta 1847(9):849–860

    Article  PubMed  Google Scholar 

  34. Boada M, Antúnez C, Ramírez-Lorca R, AL DS, González-Pérez A, Gayán J, López-Arrieta J, Ikram MA, Hernández I, Marín J, Galán JJ, Bis JC, Mauleón A, Rosende-Roca M, Moreno-Rey C, Gudnasson V, Morón FJ, Velasco J, Carrasco JM, Alegret M, Espinosa A, Vinyes G, Lafuente A, Vargas L, Fitzpatrick AL, Alzheimer’s Disease Neuroimaging Initiative, Launer LJ, Sáez ME, Vázquez E, Becker JT, López OL, Serrano-Ríos M, Tárraga L, van Duijn CM, Real LM, Seshadri S, Ruiz A (2014) ATP5H/KCTD2 locus is associated with Alzheimer’s disease risk. Mol Psychiatry 19(6):682–687

    Article  CAS  PubMed  Google Scholar 

  35. Zhu H, Chen L, Zhou W, Huang Z, Hu J, Dai S, Wang X, Huang X, He C (2013) Over-expression of the ATP5J gene correlates with cell migration and 5-fluorouracil sensitivity in colorectal cancer. PLoS One 8(10):e76846

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Brown DA, Perry JB, Allen ME, Sabbah HN, Stauffer BL, Shaikh SR, Cleland JG, Colucci WS, Butler J, Voors AA, Anker SD, Pitt B, Pieske B, Filippatos G, Greene SJ, Gheorghiade M (2016) Expert consensus document: mitochondrial function as a therapeutic target in heart failure. Nat Rev Cardiol. doi:10.1038/nrcardio.2016.203

    PubMed Central  Google Scholar 

  37. Lesnefsky EJ, Chen Q, Tandler B, Hoppel CL (2017) Mitochondrial dysfunction and myocardial ischemia-reperfusion: implications for novel therapies. Annu Rev Pharmacol Toxicol 57:535–565

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work is supported by the China National Nature Science Foundation (grant no. 31201963).

Author information

Authors and Affiliations

  1. Henan Provincial Open Laboratory of Key Disciplines, Environment and Animal Products Safety, College of Animal Science and Technology, Henan University of Science and Technology, Kaiyuan Avenue 263, Luoyang, 471000, Henan, People’s Republic of China

    Hong-wei Wang, Wen-peng Zhao, Jing Liu, Pan-pan Tan, Wei-shun Tian & Bian-hua Zhou

Authors
  1. Hong-wei Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Wen-peng Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jing Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Pan-pan Tan
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Wei-shun Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Bian-hua Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hong-wei Wang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, Hw., Zhao, Wp., Liu, J. et al. ATP5J and ATP5H Proactive Expression Correlates with Cardiomyocyte Mitochondrial Dysfunction Induced by Fluoride. Biol Trace Elem Res 180, 63–69 (2017). https://doi.org/10.1007/s12011-017-0983-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12011-017-0983-5

Keywords

Search

Navigation