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Biological Trace Element Research

, Volume 144, Issue 1–3, pp 636–646 | Cite as

High Copper Levels Promotes Broiler Hepatocyte Mitochondrial Permeability Transition In Vivo and In Vitro

  • Rongsheng Su
  • Rongmei Wang
  • Huabin Cao
  • Jiaqiang Pan
  • Lijun Chen
  • Chengmei Li
  • Dayou Shi
  • Zhaoxin Tang
Article

Abstract

This study was to examine the effects of copper on the mitochondrial non-specific pore. Three hundred sixty, one-day-old, healthy Arbor Acres (AA) broilers were fed with different concentrations (11, 110, 220, and 330 mg/kg) of copper originated from copper sulfate, tribasic copper chloride (TBCC), or copper methionine. At the indicated time point, the mitochondrial permeability transition (MPT) and copper concentration were analyzed. Results showed that under the same copper concentration, the MPT of broilers fed copper methionine was the greatest, followed by TBCC, then copper sulfate. The effects of copper on MPT were time- and dose-dependent. Furthermore, in vitro in the presence of K+, 5 μM Cu2+ could cause permeability transition as compared to 10 μM Cu2+ in buffer without K+. Taking these results together, we have shown that hepatocellular MPT may be influenced not only by source and concentration of copper or the raising period of broilers, but also by the existence of K+.

Keywords

Copper Broiler Mitochondria Mitochondrial permeability transition 

Notes

Acknowledgements

This project was supported by the National Natural Science Foundation of China (No.30871900).

References

  1. 1.
    Mertz W (1987) Trace elements in human and animal nutrition, 5th edn. Academic, Orlando, pp 301–350Google Scholar
  2. 2.
    Chuttani HK, Gupta PS, Gulati S, Gupta DN (1965) Acute copper sulfate poisoning. Am J Med 39:849–854PubMedCrossRefGoogle Scholar
  3. 3.
    Koizumi T, Yokota T, Shirakura H, Tatsumoto H, Suzuki KT (1994) Potential mechanism of cadmium-induced cytotoxicity in rat hepatocytes: inhibitory action of cadmium on mitochondrial respiratory activity. Toxicol 92:115–125CrossRefGoogle Scholar
  4. 4.
    Xiang LX, Shao JZ (2003) Role of intracellular Ca2+, reactive oxygen species, mitochondria transmembrane potential, and antioxidant enzymes in heavy metal-induced apoptosis in fish cell. Bull Environ Contam Toxicol 71:114–122PubMedCrossRefGoogle Scholar
  5. 5.
    Zhao M, Antunes F, Eaton JW, Brunk UT (2003) Lysosomal enzymes promote mitochondrial oxidant product, cytochrome c release and apoptosis. Eur J Biochem 270:3778–3786PubMedCrossRefGoogle Scholar
  6. 6.
    Kowaltowski AJ, Castilho RF, Grijalba MT, Bechara EJ, Vercesi AE (1996) Effect of inorganic phosphate concentration on the nature of inner mitochondrial membrane alterations mediated by Ca2+ ions. A proposed model for phosphate-stimulated lipid peroxidation. J Biol Chem 271:2929–2934PubMedCrossRefGoogle Scholar
  7. 7.
    Orrenius S, Zhivotovsky B, Nicotera P (2003) Regulation of cell death: the calcium–apoptosis link. Nat Rev Mol Cell Biol 4:552–565PubMedCrossRefGoogle Scholar
  8. 8.
    Kowaltowski AJ, Castilho RF, Vercesi AE (2001) Mitochondrial permeability transition and oxidative stress. FEBS Lett 20:12–15CrossRefGoogle Scholar
  9. 9.
    Lemasters JJ (1999) Necrapoptosis and the mitochondria permeability transition: shared pathways to necrosis and apoptosis. Am J Physiol 276:1–6Google Scholar
  10. 10.
    Britton RS (1996) Metal-induced hepatotoxicity. Lipids 16:3–12Google Scholar
  11. 11.
    Krumschnabel G, Manzi C, Berger C, Hofer B (2005) Oxidative stress, mitochondrial permeability transition in Cu-exposed trout hepatocytes. Toxicol Appl Pharmacol 209:62–73PubMedCrossRefGoogle Scholar
  12. 12.
    Bottje WG, Tang Z, Iqbal M (2002) Association of mitochondrail function with feed efficiency within a single genetic line of male broilers. Poult Sci 81:546–555PubMedGoogle Scholar
  13. 13.
    Garcia N, Zazucta C, Carrillo R, Correa F, Chavez E (2000) Copper sensitizes the mitochondrial permeability transition to cayboxytractyloside and oleate. Mol Cell Biochem 209:119–123PubMedCrossRefGoogle Scholar
  14. 14.
    Tang Z, Iqbal M, Cawthon D, Bottje WG (2002) Heart and breast muscle mitochondrial dysfunction in pulmonary hypertension syndrome in broilers (Gallus domesticus). Comp Biochem PhysiolA 132:527–540CrossRefGoogle Scholar
  15. 15.
    Bradford HF, Dodd PR (1977) Convulsions and activation of epileptic foci induced by monosodium glutamate and related compounds. Biochem Pharmacol 26:253–254PubMedCrossRefGoogle Scholar
  16. 16.
    Oliverira PJ, Coxito PM, Rolo AP, Santos DL, Palmeira CM, Moreno AJM (2001) Inhibitory effect of carvedilol in the high-conductance state of the mitochondrial permeability transition pore. Eur J Pharmcol 412:231–237CrossRefGoogle Scholar
  17. 17.
    Littell RC, Lewis AJ, Henry PR (1995) Statistical evaluation of bioavailability assays. In: Ammerman CB, Baker DH, Lewis AJ (eds) Bioavailability of nutrients for animals. Academic, San Diego, pp 5–33CrossRefGoogle Scholar
  18. 18.
    Bass DA, Parce JW, Dechatelet LR, Szejda P (1983) Flow cytometric studies of oxidative product formation by neutrophils: a graded response to membrane stimulation. J Immunol 130:1910–1915PubMedGoogle Scholar
  19. 19.
    Iqbal M, Cawthon D, Bottje WG, Rath N (2001) Lung mitochondrial dysfunction in pulmonary hypertension syndrome. I. Site-specific defects in the electron transport chain. Poult Sci 80:485–495PubMedGoogle Scholar
  20. 20.
    Garcia N, Martinez-Abundis E, Natalia P, Francisco C (2007) Copper induces permeability transition through its interaction with the adenine nucleotide translocase. Cell Biol Int 31:893–899PubMedCrossRefGoogle Scholar
  21. 21.
    Manzl C, Enrich J, Ebner H, Dallinger R, Krumschnabel G (2004) Copper-induced formation of reactive oxygen species causes cell death and disruption of calcium homeostasis in trout hepatocytes. Toxicol 196:57–64CrossRefGoogle Scholar
  22. 22.
    Chavez E, Moreno R, Zazueta C, Reyes-Vivas H, Arteaga D (1991) Intramitochondrial K+ as activator of carboxyatractyloside-induced Ca2+ release. Biochim Biophys Acta 1070:461–466PubMedCrossRefGoogle Scholar
  23. 23.
    Hunter DR, Haworth RA (1979) The Ca2+-induced membrane transition in mitochondria I The protective mechanisms. Arch Biochem Biophys 195:453–459PubMedCrossRefGoogle Scholar
  24. 24.
    Chowdhury SD, Paik IK, Namkung H, Lim HS (2004) Responses of broiler chickens to organic copper fed in the form of copper-methionine chelate. Anim Feed Sci Technol 115:281–293CrossRefGoogle Scholar
  25. 25.
    Pesti GM, Bakalli RI (1996) Studies on the feeding of cupric sulfate pentahydrate and cupric citrate to broiler chickens. Poult Sci 75:1086–1091PubMedCrossRefGoogle Scholar
  26. 26.
    Sokol RJ, Devereaux MW, O'Brien K, Khandwala RA, Loer JP (1993) Abnormal hepatic mitochondrial respiration and cytochrome c oxidase activity in rats with long-term copper overload. Gastroenterology 105:178–187PubMedGoogle Scholar
  27. 27.
    Sokol RJ, Twedt D, Mckim J, Devereaux MW, Karrer FM (1994) Oxidant injury to hepatic mitochondria in patients with Wilson's disease and Bedlington terriers with copper toxicosis. Gastroenterology 107:1788–1798PubMedGoogle Scholar
  28. 28.
    Fernandez-Checa JC, Kaplowitz N, Colell A, Miranda M, Montserrat M, Ardite E (1997) GSH transport in mitochondria: defense against TNF-induced oxidative stress and alcohol-induced defect. Am J Physiol 36:7–17Google Scholar
  29. 29.
    Glerum DA, Shtanko A, Tzagoloff A (1996) Characterization of COX17, a yeast gene involved in copper metabolism and assembly of cytochrome oxidase. J Bio Chem 271:14504–14509CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2011

Authors and Affiliations

  • Rongsheng Su
    • 1
  • Rongmei Wang
    • 2
  • Huabin Cao
    • 3
  • Jiaqiang Pan
    • 1
  • Lijun Chen
    • 1
  • Chengmei Li
    • 1
  • Dayou Shi
    • 1
  • Zhaoxin Tang
    • 1
  1. 1.College of Veterinary MedicineSouth China Agricultural UniversityGuangzhouChina
  2. 2.College of Ying Dong bio-engineeringShaoguan UniversityShaoguanChina
  3. 3.College of Animal Science and TechnologyJiangxi Agricultural UniversityNanchangChina

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