Feeding low or pharmacological concentrations of zinc oxide changes the hepatic proteome profiles in weaned piglets

PLoS ONE

Volumn 8, Issue 11, 2013, Pages

  Bondzio, Angelika ^a   Pieper, Robert ^a   Gabler, Christoph ^a   Weise, Christoph ^a   Schulze, Petra ^a   Zentek, Juergen ^a   Einspanier, Ralf ^a  

^a FREIE UNIVERSITÄT BERLIN   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; BASE SEQUENCE; DIETARY SUPPLEMENTS; DNA PRIMERS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; LIVER; PROTEOME; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; SWINE; WEANING; ZINC OXIDE;

EID: 84894229201     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0081202     Document Type: Article

References (77)

1. Suttle N (2010) Mineral Nutrition of Livestock, 4th Edition Preface. Mineral Nutrition of Livestock, 4th Edition: Vii-Viii.
2. Chasapis CT, Loutsidou AC, Spiliopoulou CA, Stefanidou ME (2012) Zinc and human health: an update. Arch Toxicol 86: 521-534.
3. Krebs NF (2013) Update on Zinc Deficiency and Excess in Clinical Pediatric Practice. Annals of Nutrition and Metabolism 62: 19-29.
4. Hahn JD, Baker DH (1993) Growth and plasma zinc responses of young pigs fed pharmacologic levels of zinc. J Anim Sci 71: 3020-3024.
5. Case CL, Carlson MS (2002) Effect of feeding organic and inorganic sources of additional zinc on growth performance and zinc balance in nursery pigs. J Anim Sci 80: 1917-1924.
6. Hu C, Song J, You Z, Luan Z, Li W (2012) Zinc oxide-montmorillonite hybrid influences diarrhea, intestinal mucosal integrity, and digestive enzyme activity in weaned pigs. Biol Trace Elem Res 149: 190-196.
7. Poulsen HD (1995) Zinc-Oxide for Weanling Piglets. Acta Agriculturae Scandinavica Section a-Animal Science 45: 159-167.
8. Wang X, Ou D, Yin J, Wu G, Wang J (2009) Proteomic analysis reveals altered expression of proteins related to glutathione metabolism and apoptosis in the small intestine of zinc oxide-supplemented piglets. Amino Acids 37: 209-218.
9. Hojberg O, Canibe N, Poulsen HD, Hedemann MS, Jensen BB (2005) Influence of dietary zinc oxide and copper sulfate on the gastrointestinal ecosystem in newly weaned piglets. Appl Environ Microbiol 71: 2267-2277.
10. Vahjen W, Pieper R, Zentek J (2011) Increased dietary zinc oxide changes the bacterial core and enterobacterial composition in the ileum of piglets. J Anim Sci 89: 2430-2439.
11. Zhang B, Guo Y (2009) Supplemental zinc reduced intestinal permeability by enhancing occludin and zonula occludens protein-1 (ZO-1) expression in weaning piglets. Br J Nutr 102: 687-693.
12. Hu C, Song J, Li Y, Luan Z, Zhu K (2013) Diosmectite-zinc oxide composite improves intestinal barrier function, modulates expression of pro-inflammatory cytokines and tight junction protein in early weaned pigs. Br J Nutr: 1-8.
13. Li X, Yin J, Li D, Chen X, Zang J, et al. (2006) Dietary supplementation with zinc oxide increases Igf-I and Igf-I receptor gene expression in the small intestine of weanling piglets. J Nutr 136: 1786-1791.
14. Yin J, Li X, Li D, Yue T, Fang Q, et al. (2009) Dietary supplementation with zinc oxide stimulates ghrelin secretion from the stomach of young pigs. J Nutr Biochem 20: 783-790.
15. Lichten LA, Cousins RJ (2009) Mammalian zinc transporters: nutritional and physiologic regulation. Annu Rev Nutr 29: 153-176.
16. Schell TC, Kornegay ET (1996) Zinc concentration in tissues and performance of weanling pigs fed pharmacological levels of zinc from ZnO, Zn-methionine, Zn-lysine, or ZnSO4. J Anim Sci 74: 1584-1593.
17. Carlson MS, Hill GM, Link JE (1999) Early- and traditionally weaned nursery pigs benefit from phase-feeding pharmacological concentrations of zinc oxide: effect on metallothionein and mineral concentrations. J Anim Sci 77: 1199-1207.
18. Martinez MM, Hill GM, Link JE, Raney NE, Tempelman RJ, et al. (2004) Pharmacological zinc and phytase supplementation enhance metallothionein mRNA abundance and protein concentration in newly weaned pigs. J Nutr 134: 538-544.
19. Martinez MM, Link JE, Hill GM (2005) Dietary pharmacological or excess zinc and phytase effects on tissue mineral concentrations, metallothionein, and apparent mineral retention in the newly weaned pig. Biol Trace Elem Res 105: 97-115.
20. Stamoulis I, Kouraklis G, Theocharis S (2007) Zinc and the liver: an active interaction. Dig Dis Sci 52: 1595-1612.
21. Martinez-Montemayor MM, Hill GM, Raney NE, Rilington VD, Tempelman RJ, et al. (2008) Gene expression profiling in hepatic tissue of newly weaned pigs fed pharmacological zinc and phytase supplemented diets. BMC Genomics 9: 421.
22. Bondzio A, Gabler C, Badewien-Rentzsch B, Schulze P, Martens H, et al. (2011) Identification of differentially expressed proteins in ruminal epithelium in response to a concentrate-supplemented diet. Am J Physiol Gastrointest Liver Physiol 301: G260-268.
23. Pieper R, Vahjen W, Neumann K, Van Kessel AG, Zentek J (2012) Dose-dependent effects of dietary zinc oxide on bacterial communities and metabolic profiles in the ileum of weaned pigs. J Anim Physiol Anim Nutr (Berl) 96: 825-833.
24. Marouga R, David S, Hawkins E (2005) The development of the DIGE system: 2D fluorescence difference gel analysis technology. Anal Bioanal Chem 382: 669-678.
25. Shevchenko A, Wilm M, Vorm O, Mann M (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal Chem 68: 850-858.
26. Martin L, Lodemann U, Bondzio A, Gefeller EM, Vahjen W, et al. (2013) A High Amount of Dietary Zinc Changes the Expression of Zinc Transporters and Metallothionein in Jejunal Epithelial Cells in Vitro and in Vivo but Does Not Prevent Zinc Accumulation in Jejunal Tissue of Piglets. J Nutr.
27. Odau S, Gabler C, Holder C, Einspanier R (2006) Differential expression of cyclooxygenase 1 and cyclooxygenase 2 in the bovine oviduct. J Endocrinol 191: 263-274.
28. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, et al. (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3: RESEARCH0034.
29. Carlson D, Sehested J, Feng Z, Poulsen HD (2008) Serosal zinc attenuate serotonin and vasoactive intestinal peptide induced secretion in piglet small intestinal epithelium in vitro. Comp Biochem Physiol A Mol Integr Physiol 149: 51-58.
30. Hill GM, Mahan DC, Carter SD, Cromwell GL, Ewan RC, et al. (2001) Effect of pharmacological concentrations of zinc oxide with or without the inclusion of an antibacterial agent on nursery pig performance. J Anim Sci 79: 934-941.
31. Cousins RJ, Liuzzi JP, Lichten LA (2006) Mammalian zinc transport, trafficking, and signals. J Biol Chem 281: 24085-24089.
32. Wang X, Li H, Fan Z, Liu Y (2012) Effect of zinc supplementation on type 2 diabetes parameters and liver metallothionein expressions in Wistar rats. J Physiol Biochem 68: 563-572.
33. Beattie JH, Gordon MJ, Reid MD, Rucklidge GJ, Kwon CS, et al. (2006) Hepatic responses to dietary stress in zinc- and metallothionein-deficient mice. Exp Biol Med (Maywood) 231: 1542-1547.
34. El Hendy HA, Yousef MI, Abo El-Naga NI (2001) Effect of dietary zinc deficiency on hematological and biochemical parameters and concentrations of zinc, copper, and iron in growing rats. Toxicology 167: 163-170.
35. Yousef MI, El-Hendy HA, El-Demerdash FM, Elagamy EI (2002) Dietary zinc deficiency induced-changes in the activity of enzymes and the levels of free radicals, lipids and protein electrophoretic behavior in growing rats. Toxicology 175: 223-234.
36. Wu JY, Reaves SK, Wang YR, Wu Y, Lei PP, et al. (1998) Zinc deficiency decreases plasma level and hepatic mRNA abundance of apolipoprotein A-I in rats and hamsters. Am J Physiol 275: C1516-1525.
37. Wu JY, Wu Y, Reaves SK, Wang YR, Lei PP, et al. (1999) Apolipoprotein A-I gene expression is regulated by cellular zinc status in hep G2 cells. Am J Physiol 277: C537-544.
38. Cui L, Schoene NW, Zhu L, Fanzo JC, Alshatwi A, et al. (2002) Zinc depletion reduced Egr-1 and HNF-3beta expression and apolipoprotein A-I promoter activity in Hep G2 cells. Am J Physiol Cell Physiol 283: C623-630.
39. Urani C, Melchioretto P, Gribaldo L (2010) Regulation of metallothioneins and ZnT-1 transporter expression in human hepatoma cells HepG2 exposed to zinc and cadmium. Toxicol In Vitro 24: 370-374.
40. Theil EC (2004) Iron, ferritin, and nutrition. Annu Rev Nutr 24: 327-343.
41. Quarles CD, Jr., Brumaghim JL, Marcus RK (2010) Simultaneous multiple element detection by particle beam/hollow cathode-optical emission spectroscopy as a tool for metallomic studies: determinations of metal binding with apotransferrin. Metallomics 2: 154-161.
42. Evans GW (1976) Transferrin function in zinc absorption and transport. Proc Soc Exp Biol Med 151: 775-778.
43. Gutteridge JM, Quinlan GJ (1993) Antioxidant protection against organic and inorganic oxygen radicals by normal human plasma: the important primary role for iron-binding and iron-oxidising proteins. Biochim Biophys Acta 1156: 144-150.
44. Perry DK, Smyth MJ, Stennicke HR, Salvesen GS, Duriez P, et al. (1997) Zinc is a potent inhibitor of the apoptotic protease, caspase-3. A novel target for zinc in the inhibition of apoptosis. J Biol Chem 272: 18530-18533.
45. Zhou Z, Liu J, Song Z, McClain CJ, Kang YJ (2008) Zinc supplementation inhibits hepatic apoptosis in mice subjected to a long-term ethanol exposure. Exp Biol Med (Maywood) 233: 540-548.
46. Nakatani T, Tawaramoto M, Opare Kennedy D, Kojima A, Matsui-Yuasa I (2000) Apoptosis induced by chelation of intracellular zinc is associated with depletion of cellular reduced glutathione level in rat hepatocytes. Chem Biol Interact 125: 151-163.
47. Cao J, Bobo JA, Liuzzi JP, Cousins RJ (2001) Effects of intracellular zinc depletion on metallothionein and ZIP2 transporter expression and apoptosis. J Leukoc Biol 70: 559-566.
48. Mukhopadhyay I, Nazir A, Saxena DK, Chowdhuri DK (2003) Heat shock response: hsp70 in environmental monitoring. J Biochem Mol Toxicol 17: 249-254.
49. Zhong X, Li W, Huang X, Zhang L, Yimamu M, et al. (2012) Impairment of cellular immunity is associated with overexpression of heat shock protein 70 in neonatal pigs with intrauterine growth retardation. Cell Stress Chaperones 17: 495-505.
50. Hartl FU, Hayer-Hartl M (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295: 1852-1858.
51. Arya R, Mallik M, Lakhotia SC (2007) Heat shock genes - integrating cell survival and death. J Biosci 32: 595-610.
52. Lodemann U, Einspanier R, Scharfen F, Martens H, Bondzio A (2013) Effects of zinc on epithelial barrier properties and viability in a human and a porcine intestinal cell culture model. Toxicol In Vitro 27: 834-843.
53. Van Molle W, Van Roy M, Van Bogaert T, Dejager L, Van Lint P, et al. (2007) Protection of zinc against tumor necrosis factor induced lethal inflammation depends on heat shock protein 70 and allows safe antitumor therapy. Cancer Res 67: 7301-7307.
54. Soti C, Csermely P (2003) Aging and molecular chaperones. Exp Gerontol 38: 1037-1040.
55. Zhang M, Lv Y, Yue Z, Islam A, Rehana B, et al. (2011) Effects of transportation on expression of Hsp90, Hsp70, Hsp27 and alpha B-crystallin in the pig stomach. Veterinary Record 169: 312-U356.
56. Mkrtchian S, Sandalova T (2006) ERp29, an unusual redox-inactive member of the thioredoxin family. Antioxid Redox Signal 8: 325-337.
57. Zhang D, Richardson DR (2011) Endoplasmic reticulum protein 29 (ERp29): An emerging role in cancer. Int J Biochem Cell Biol 43: 33-36.
58. Sargsyan E, Baryshev M, Szekely L, Sharipo A, Mkrtchian S (2002) Identification of ERp29, an endoplasmic reticulum lumenal protein, as a new member of the thyroglobulin folding complex. J Biol Chem 277: 17009-17015.
59. Cook T, Gebelein B, Urrutia R (1999) Sp1 and its likes: biochemical and functional predictions for a growing family of zinc finger transcription factors. Ann N Y Acad Sci 880: 94-102.
60. Ragg H (2007) The role of serpins in the surveillance of the secretory pathway. Cell Mol Life Sci 64: 2763-2770.
61. Park KJ, Kim HY, Chang BJ, Lee HH (2004) Ameliorative effects of soy 11S protein on liver damage and hyperlipidemia in alcohol-fed rats. Biol Pharm Bull 27: 1636-1641.
62. Nagata H, Ito M, Cai J, Edge AS, Platt JL, et al. (2003) Treatment of cirrhosis and liver failure in rats by hepatocyte xenotransplantation. Gastroenterology 124: 422-431.
63. Jobgen WS, Fried SK, Fu WJ, Meininger CJ, Wu G (2006) Regulatory role for the arginine-nitric oxide pathway in metabolism of energy substrates. J Nutr Biochem 17: 571-588.
64. She YM, Narindrasorasak S, Yang S, Spitale N, Roberts EA, et al. (2003) Identification of metal-binding proteins in human hepatoma lines by immobilized metal affinity chromatography and mass spectrometry. Mol Cell Proteomics 2: 1306-1318.
65. Brand IA, Kleineke J (1996) Intracellular zinc movement and its effect on the carbohydrate metabolism of isolated rat hepatocytes. J Biol Chem 271: 1941-1949.
66. Rofe AM, Philcox JC, Coyle P (2000) Activation of glycolysis by zinc is diminished in hepatocytes from metallothionein-null mice. Biol Trace Elem Res 75: 87-97.
67. Zhu Y, Goodridge AG, Stapleton SR (1994) Zinc, Vanadate and Selenate Inhibit the Tri-Iodothyronine-Induced Expression of Fatty-Acid Synthase and Malic Enzyme in Chick-Embryo Hepatocytes in Culture. Biochemical Journal 303: 213-216.
68. Hung HC, Chang GG, Yang ZR, Tong L (2000) Slow binding of metal ions to pigeon liver malic enzyme: A general case. Biochemistry 39: 14095-14102.
69. Sandstead HH, Frederickson CJ, Penland JG (2000) History of zinc as related to brain function. Journal of Nutrition 130: 496s-502s.
70. Halsted CH, Villanueva JA, Devlin AM, Niemela O, Parkkila S, et al. (2002) Folate deficiency disturbs hepatic methionine metabolism and promotes liver injury in the ethanol-fed micropig. Proc Natl Acad Sci U S A 99: 10072-10077.
71. Zhou Z, Wang L, Song Z, Saari JT, McClain CJ, et al. (2005) Zinc supplementation prevents alcoholic liver injury in mice through attenuation of oxidative stress. Am J Pathol 166: 1681-1690.
72. Cossack ZT, Prasad AS (1991) Activities of Purine Catabolism Related Enzymes in Zinc-Deficiency - Relationship to T-Lymphocyte Dysfunction and Hyperammonemia. International Journal for Vitamin and Nutrition Research 61: 51-56.
73. Aminlari M, Li A, Kunanithy V, Scaman CH (2002) Rhodanese distribution in porcine (Sus scrofa) tissues. Comp Biochem Physiol B Biochem Mol Biol 132: 309-313.
74. Himwich WA, Saunders JP (1948) Enzymatic Conversion of Cyanide to Thiocyanate. American Journal of Physiology 153: 348-354.
75. Cipollone R, Ascenzi P, Visca P (2007) Common themes and variations in the rhodanese superfamily. IUBMB Life 59: 51-59.
76. Volini M, Van Sweringen B, Chen FS (1978) Effects of metal-ion binding on rhodanese activity. Arch Biochem Biophys 191: 205-215.
77. Lee GD, Lee MH, Ihm J (1995) Role of d electrons in the zinc-blende semiconductors ZnS, ZnSe, and ZnTe. Phys Rev B Condens Matter 52: 1459-1462.