Proteomic analysis shows the upregulation of erythrocyte dematin in zinc-restricted human subjects

American Journal of Clinical Nutrition

Volumn 95, Issue 5, 2012, Pages 1096-1102

  Ryu, Moon Suhn ^a   Guthrie, Gregory J ^a   Maki, Alyssa B ^a   Aydemir, Tolunay B ^a   Cousins, Robert J ^a  

^a UNIVERSITY OF FLORIDA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ERYTHROCYTE BAND 4.9 PROTEIN; PROTEIN ZIP10; PROTEIN ZIP8; UNCLASSIFIED DRUG; ZINC; ZINC TRANSPORTER; ZINC TRANSPORTER 1;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CYTOSKELETON; DIET RESTRICTION; DIETARY INTAKE; ERYTHROCYTE MEMBRANE; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; MALE; MOLECULAR WEIGHT; MOUSE; NONHUMAN; NORMAL HUMAN; OBSERVATIONAL STUDY; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS; UPREGULATION; ZINC INTAKE; ZINC RESTRICTION;

ADULT; AMINO ACID SEQUENCE; ANIMALS; BIOLOGICAL MARKERS; BLOTTING, WESTERN; CARRIER PROTEINS; CATION TRANSPORT PROTEINS; ERYTHROCYTES; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICROFILAMENT PROTEINS; MOLECULAR SEQUENCE DATA; NUTRITIONAL STATUS; PROTEOME; TANDEM MASS SPECTROMETRY; UP-REGULATION; YOUNG ADULT; ZINC;

MUS;

EID: 84860273366     PISSN: 00029165     EISSN: 19383207     Source Type: Journal    
DOI: 10.3945/ajcn.111.032862     Document Type: Article

References (44)

1. Ohno H, Doi R, Yamamura K, Yamashita K, Iizuka S, Taniguchi N. A study of zinc distribution in erythrocytes of normal humans. Blut 1985;50:113-6. (Pubitemid 15143880)
2. Grider A, Bailey LB, Cousins RJ. Erythrocyte metallothionein as an index of zinc status in humans. Proc Natl Acad Sci USA 1990;87:1259-62.
3. Ryu MS, Lichten LA, Liuzzi JP, Cousins RJ. Zinc transporters ZnT1 (Slc30a1), Zip8 (Slc39a8), and Zip10 (Slc39a10) in mouse red blood cells are differentially regulated during erythroid development and by dietary zinc deficiency. J Nutr 2008;138:2076-83.
4. Thomas EA, Bailey LB, Kauwell GA, Lee DY, Cousins RJ. Erythrocyte metallothionein response to dietary zinc in humans. J Nutr 1992;122:2408-14. (Pubitemid 23004639)
5. Bloomer JR, Reuter RJ, Morton KO, Wehner JM. Enzymatic formation of zinc-protoporphyrin by rat liver and its potential effect on hepatic heme metabolism. Gastroenterology 1983;85:663-8. (Pubitemid 13033126)
6. O'Dell BL, Browning JD, Reeves PG. Zinc deficiency increases the osmotic fragility of rat erythrocytes. J Nutr 1987;117:1883-9. (Pubitemid 18015394)
7. Woodhouse LR, Lederer LJ, Lowe NM, King JC. The effects of zinc status on the osmotic fragility of human erythrocytes. In: Fischer PWF, Abbe MR, Cockell KA, Gibson RS, eds. Trace elements in man and animals-9. Proceedings of the Ninth International Symposium on Trace Elements on Man and Animals. Ottawa, Canada: NRC Research Press, 1997:636-8.
8. King JC. Zinc: an essential but elusive nutrient. Am J Clin Nutr 2011;94(suppl):679S-84S.
9. Khanna R, Chang SH, Andrabi S, Azam M, Kim A, Rivera A, Brugnara C, Low PS, Liu SC, Chishti AH. Headpiece domain of dematin is required for the stability of the erythrocyte membrane. Proc Natl Acad Sci USA 2002;99:6637-42. (Pubitemid 34526185)
10. Chen H, Khan AA, Liu F, Gilligan DM, Peters LL, Messick J, Haschek-Hock WM, Li X, Ostafin AE, Chishti AH. Combined deletion of mouse dematin-headpiece and beta-adducin exerts a novel effect on the spectrin-actin junctions leading to erythrocyte fragility and hemolytic anemia. J Biol Chem 2007;282:4124-35. (Pubitemid 47084499)
11. Hedera P, Peltier A, Fink JK, Wilcock S, London Z, Brewer GJ. Myelopolyneuropathy and pancytopenia due to copper deficiency and high zinc levels of unknown origin II. The denture cream is a primary source of excessive zinc. Neurotoxicology 2009;30:996-9.
12. Gordon PR, Woodruff CW, Anderson HL, O'Dell BL. Effect of acute zinc deprivation on plasma zinc and platelet aggregation in adult males. Am J Clin Nutr 1982;35:113-9. (Pubitemid 12126595)
13. Ryu MS, Langkamp-Henken B, Chang SM, Shankar MN, Cousins RJ. Genomic analysis, cytokine expression, and microRNA profiling reveal biomarkers of human dietary zinc depletion and homeostasis. Proc Natl Acad Sci USA 2011;108:20970-5.
14. King JC, Shames DM, Lowe NM, Woodhouse LR, Sutherland B, Abrams SA, Turnlund JR, Jackson MJ. Effect of acute zinc depletion on zinc homeostasis and plasma zinc kinetics in men. Am J Clin Nutr 2001;74:116-24. (Pubitemid 32574919)
15. Bonafoux B, Commes T. Serial analysis of gene expression adapted for downsized extracts (SAGE/SADE) analysis in reticulocytes. Methods Mol Biol 2009;496:299-311.
16. McMahon RJ, Cousins RJ. Regulation of the zinc transporter ZnT-1 by dietary zinc. Proc Natl Acad Sci USA 1998;95:4841-6. (Pubitemid 28208513)
17. Aydemir TB, Liuzzi JP, McClellan S, Cousins RJ. Zinc transporter ZIP8 (SLC39A8) and zinc influence IFN-gamma expression in activated human T cells. J Leukoc Biol 2009;86:337-48.
18. Lichten LA, Ryu MS, Guo L, Embury J, Cousins RJ. MTF-1-mediated repression of the zinc transporter Zip10 is alleviated by zinc restriction. PLoS ONE 2011;6:e21526.
19. Aydemir TB, Blanchard RK, Cousins RJ. Zinc supplementation of young men alters metallothionein, zinc transporter, and cytokine gene expression in leukocyte populations. Proc Natl Acad Sci USA 2006;103:1699-704. (Pubitemid 43228756)
20. Ferreira R, Ohneda K, Yamamoto M, Philipsen S. GATA1 function, a paradigm for transcription factors in hematopoiesis. Mol Cell Biol 2005;25:1215-27. (Pubitemid 40204902)
21. Hodge D, Coghill E, Keys J, Maguire T, Hartmann B, McDowall A, Weiss M, Grimmond S, Perkins A. A global role for EKLF in definitive and primitive erythropoiesis. Blood 2006;107:3359-70.
22. Naber TH, van den Hamer CJ, van den Broek WJ, van Tongeren JH. Zinc uptake by blood cells of rats in zinc deficiency and inflammation. Biol Trace Elem Res 1992;35:137-52.
23. Van Wouwe JP, Veldhuizen M, De Goeij JJ, Van den Hamer CJ. Laboratory assessment of early dietary, subclinical zinc deficiency: a model study on weaning rats. Pediatr Res 1991;29:391-5.
24. Chesters JK, Will M. The assessment of zinc status of an animal from the uptake of 65Zn by the cells of whole blood in vitro. Br J Nutr 1978;39:297-306. (Pubitemid 8281991)
25. Langmade SJ, Ravindra R, Daniels PJ, Andrews GK. The transcription factor MTF-1 mediates metal regulation of the mouse ZnT1 gene. J Biol Chem 2000;275:34803-9.
26. Zheng D, Feeney GP, Kille P, Hogstrand C. Regulation of ZIP and ZnT zinc transporters in zebrafish gill: zinc repression of ZIP10 transcription by an intronic MRE cluster. Physiol Genomics 2008;34:205-14.
27. Glader B. Destruction of erythrocytes. In: Greer JP, Foerster J, Rodgers GM, Paraskevas F, Glader B, eds. Wintrobe's clinical hematology. Philadelphia, PA: Lippincott Williams & Wilkins, 2008:156-69.
28. Siegel DL, Branton D. Partial purification and characterization of an actin-bundling protein, band 4.9, from human erythrocytes. J Cell Biol 1985;100:775-85. (Pubitemid 15135337)
29. Rana AP, Ruff P, Maalouf GJ, Speicher DW, Chishti AH. Cloning of human erythroid dematin reveals another member of the villin family. Proc Natl Acad Sci USA 1993;90:6651-5. (Pubitemid 23207271)
30. Salomao M, Zhang X, Yang Y, Lee S, Hartwig JH, Chasis JA, Mohandas N, An X. Protein 4.1R-dependent multiprotein complex: new insights into the structural organization of the red blood cell membrane. Proc Natl Acad Sci USA 2008;105:8026-31. (Pubitemid 351904701)
31. Anong WA, Franco T, Chu H, Weis TL, Devlin EE, Bodine DM, An X, Mohandas N, Low PS. Adducin forms a bridge between the erythrocyte membrane and its cytoskeleton and regulates membrane cohesion. Blood 2009;114:1904-12.
32. Husain-Chishti A, Levin A, Branton D. Abolition of actin-bundling by phosphorylation of human erythrocyte protein 4.9. Nature 1988;334:718-21.
33. Tsukamoto T, Suyama K, Germann P, Sonenberg M. Adenosine cyclic 3′,5′-monophosphate uptake and regulation of membrane protein kinase in intact human erythrocytes. Biochemistry 1980;19:918-24. (Pubitemid 10112239)
34. Husain-Chishti A, Faquin W, Wu CC, Branton D. Purification of erythrocyte dematin (protein 4.9) reveals an endogenous protein kinase that modulates actin-bundling activity. J Biol Chem 1989;264:8985-91. (Pubitemid 19151626)
35. Frank BS, Vardar D, Chishti AH, McKnight CJ. The NMR structure of dematin headpiece reveals a dynamic loop that is conformationally altered upon phosphorylation at a distal site. J Biol Chem 2004;279:7909-16. (Pubitemid 38294678)
36. Donnelly TE Jr. Effects of zinc chloride on the hydrolysis of cyclic GMP and cyclic AMP by the activator-dependent cyclic nucleotide phosphodiesterase from bovine heart. Biochim Biophys Acta 1978;522:151-60.
37. von Bülow V, Dubben S, Engelhardt G, Hebel S, Plumakers B, Heine H, Rink L, Haase H. Zinc-dependent suppression of TNF-alpha production is mediated by protein kinase A-induced inhibition of Raf-1, I kappa B kinase beta, and NF-kappa B. J Immunol 2007;179:4180-6.
38. Brautigan DL, Bornstein P, Gallis B. Phosphotyrosyl-protein phosphatase. Specific inhibition by Zn. J Biol Chem 1981;256:6519-22.
39. Ho Y, Samarasinghe R, Knoch ME, Lewis M, Aizenman E, DeFranco DB. Selective inhibition of mitogen-activated protein kinase phosphatases by zinc accounts for extracellular signal-regulated kinase 1/2-dependent oxidative neuronal cell death. Mol Pharmacol 2008;74:1141-51.
40. Yamasaki S, Sakata-Sogawa K, Hasegawa A, Suzuki T, Kabu K, Sato E, Kurosaki T, Yamashita S, Tokunaga M, Nishida K, et al. Zinc is a novel intracellular second messenger. J Cell Biol 2007;177:637-45. (Pubitemid 46799835)
41. Larsson C. Protein kinase C and the regulation of the actin cytoskeleton. Cell Signal 2006;18:276-84. (Pubitemid 41661343)
42. Csermely P, Szamel M, Resch K, Somogyi J. Zinc can increase the activity of protein kinase C and contributes to its binding to plasma membranes in T lymphocytes. J Biol Chem 1988;263:6487-90.
43. Lutchman M, Pack S, Kim AC, Azim A, Emmert-Buck M, van Huffel C, Zhuang Z, Chishti AH. Loss of heterozygosity on 8p in prostate cancer implicates a role for dematin in tumor progression. Cancer Genet Cytogenet 1999;115:65-9. (Pubitemid 29505222)
44. O'Dell BL. Role of zinc in plasma membrane function. J Nutr 2000;130(suppl):1432S-6S. (Pubitemid 30244142)