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Comparative Response of Cardiomyocyte ZIPs and ZnTs to Extracellular Zinc and TPEN

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Abstract

Intracellular zinc concentrations are tightly regulated by the coordinated regulation of ZIPs and ZnTs. Very little is known about the regulation of these transporters in cardiomyocytes, in response to extracellular zinc. Adult rat cardiomyocytes express ZnTs 1, 2, 5, and 9, in addition to ZIPs 1, 2, 3, 6, 7, 9, 10, 11, 13, and 14. We have determined the intracellular free zinc levels using Zinpyr-1 fluorescence and studied response of ZIP and ZnT mRNA by real-time PCR to the changes in extracellular zinc and TPEN in adult rat ventricular myocytes. TPEN downregulated ZnT1, ZnT2, and ZIP11 mRNAs but upregulated ZnT5, ZIP2, ZIP7, ZIP10, ZIP13, and ZIP14 mRNAs. Zinc supplementation upregulated ZnT1, ZnT2 mRNA but downregulated ZnT5, ZIP1, ZIP2, ZIP3, ZIP7, ZIP9, and ZIP10 mRNA. The negative regulation of ZIPs by zinc excess can be explained in terms of zinc homeostasis as these transporters may act to protect cells from zinc over accumulation by reducing zinc influx when the extracellular concentration of zinc is high. Similarly, the ZnT expression appears to be regulated to avoid loss of zinc from the intracellular milieu, under zinc-deficient conditions.

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References

  1. Kown MH, Van der Steenhoven T, Blankenberg FG, Hoyt G, Berry GJ, Tait JF, Strauss HW, Robbins RC (2000) Zinc-mediated reduction of apoptosis in cardiac allografts. Circulation 102(19 Suppl 3):III228–III232

    CAS  PubMed  Google Scholar 

  2. Auld DS (2001) Zinc coordination sphere in biochemical zinc sites. Biometals 14(3–4):271–313

    Article  CAS  PubMed  Google Scholar 

  3. Maret W (2011) Metals on the move: zinc ions in cellular regulation and in the coordination dynamics of zinc proteins. Biometals 24(3):411–418. https://doi.org/10.1007/s10534-010-9406-1

    Article  CAS  PubMed  Google Scholar 

  4. Coyle P, Philcox JC, Carey LC, Rofe AM (2002) Metallothionein: the multipurpose protein. Cell Mol Life Sci 59(4):627–647

    Article  CAS  PubMed  Google Scholar 

  5. Coudray C, Charlon V, de Leiris J, Favier A (1993) Effect of zinc deficiency on lipid peroxidation status and infarct size in rat hearts. Int J Cardiol 41(2):109–113

    Article  CAS  PubMed  Google Scholar 

  6. Turan B, Fliss H, Desilets M (1997) Oxidants increase intracellular free Zn2+ concentration in rabbit ventricular myocytes. Am J Phys 272(5 Pt 2):H2095–H2106. https://doi.org/10.1152/ajpheart.1997.272.5.H2095

    Article  CAS  Google Scholar 

  7. Tuncay E, Bilginoglu A, Sozmen NN, Zeydanli EN, Ugur M, Vassort G, Turan B (2011) Intracellular free zinc during cardiac excitation-contraction cycle: calcium and redox dependencies. Cardiovasc Res 89(3):634–642. https://doi.org/10.1093/cvr/cvq352

    Article  CAS  PubMed  Google Scholar 

  8. Tuncay E, Turan B (2016) Intracellular Zn(2+) increase in cardiomyocytes induces both electrical and mechanical dysfunction in heart via endogenous generation of reactive nitrogen species. Biol Trace Elem Res 169(2):294–302. https://doi.org/10.1007/s12011-015-0423-3

    Article  CAS  PubMed  Google Scholar 

  9. Lichten LA, Cousins RJ (2009) Mammalian zinc transporters: nutritional and physiologic regulation. Annu Rev Nutr 29:153–176. https://doi.org/10.1146/annurev-nutr-033009-083312

    Article  PubMed  Google Scholar 

  10. Kambe T, Tsuji T, Hashimoto A, Itsumura N (2015) The physiological, biochemical, and molecular roles of zinc transporters in zinc homeostasis and metabolism. Physiol Rev 95(3):749–784. https://doi.org/10.1152/physrev.00035.2014

    Article  CAS  PubMed  Google Scholar 

  11. Bodiga VL, Thokala S, Kovur SM, Bodiga S (2017) Zinc dyshomeostasis in cardiomyocytes after acute hypoxia/reoxygenation. Biol Trace Elem Res 179(1):117–129. https://doi.org/10.1007/s12011-017-0957-7

    Article  CAS  PubMed  Google Scholar 

  12. Crawford AJ, Bhattacharya SK (1987) Excessive intracellular zinc accumulation in cardiac and skeletal muscles of dystrophic hamsters. Exp Neurol 95(2):265–276

    Article  CAS  PubMed  Google Scholar 

  13. Lin CL, Tseng HC, Chen RF, Chen WP, Su MJ, Fang KM, Wu ML (2011) Intracellular zinc release-activated ERK-dependent GSK-3beta-p53 and Noxa-Mcl-1 signaling are both involved in cardiac ischemic-reperfusion injury. Cell Death Differ 18(10):1651–1663. https://doi.org/10.1038/cdd.2011.80

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Kasi V, Bodiga S, Kommuguri UN, Sankuru S, Bodiga VL (2011) Zinc pyrithione salvages reperfusion injury by inhibiting NADPH oxidase activation in cardiomyocytes. Biochem Biophys Res Commun 410(2):270–275. https://doi.org/10.1016/j.bbrc.2011.05.130

    Article  CAS  PubMed  Google Scholar 

  15. Viswanath K, Bodiga S, Balogun V, Zhang A, Bodiga VL (2011) Cardioprotective effect of zinc requires ErbB2 and Akt during hypoxia/reoxygenation. Biometals 24(1):171–180. https://doi.org/10.1007/s10534-010-9371-8

    Article  CAS  PubMed  Google Scholar 

  16. Karagulova G, Yue Y, Moreyra A, Boutjdir M, Korichneva I (2007) Protective role of intracellular zinc in myocardial ischemia/reperfusion is associated with preservation of protein kinase C isoforms. J Pharmacol Exp Ther 321(2):517–525. https://doi.org/10.1124/jpet.107.119644

    Article  CAS  PubMed  Google Scholar 

  17. Chanoit G, Lee S, Xi J, Zhu M, McIntosh RA, Mueller RA, Norfleet EA, Xu Z (2008) Exogenous zinc protects cardiac cells from reperfusion injury by targeting mitochondrial permeability transition pore through inactivation of glycogen synthase kinase-3beta. Am J Physiol Heart Circ Physiol 295(3):H1227–H1233. https://doi.org/10.1152/ajpheart.00610.2008

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Lee S, Chanoit G, McIntosh R, Zvara DA, Xu Z (2009) Molecular mechanism underlying Akt activation in zinc-induced cardioprotection. Am J Physiol Heart Circ Physiol 297(2):H569–H575. https://doi.org/10.1152/ajpheart.00293.2009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Baltaci AK, Yuce K (2018) Zinc transporter proteins. Neurochem Res 43(3):517–530. https://doi.org/10.1007/s11064-017-2454-y

    Article  CAS  PubMed  Google Scholar 

  20. Baltaci AK, Yuce K, Mogulkoc R (2018) Zinc metabolism and metallothioneins. Biol Trace Elem Res 183(1):22–31. https://doi.org/10.1007/s12011-017-1119-7

    Article  CAS  PubMed  Google Scholar 

  21. Reeves PG, Nielsen FH, Fahey GC Jr (1993) AIN-93 purified diets for laboratory rodents: final report of the American Institute of Nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr 123(11):1939–1951. https://doi.org/10.1093/jn/123.11.1939

    Article  CAS  PubMed  Google Scholar 

  22. Berger HJ, Prasad SK, Davidoff AJ, Pimental D, Ellingsen O, Marsh JD, Smith TW, Kelly RA (1994) Continual electric field stimulation preserves contractile function of adult ventricular myocytes in primary culture. Am J Phys 266(1 Pt 2):H341–H349. https://doi.org/10.1152/ajpheart.1994.266.1.H341

    Article  CAS  Google Scholar 

  23. Yu Z, Quamme GA, McNeill JH (1994) Depressed [Ca2+]i responses to isoproterenol and cAMP in isolated cardiomyocytes from experimental diabetic rats. Am J Phys 266(6 Pt 2):H2334–H2342

    CAS  Google Scholar 

  24. Smith RM, Martell AE, Motekaitis RJ, Standard Reference Data p (2004) NIST critically selected stability constants of metal complexes database. Standard Reference Data Program, National Institute of Standards and Technology, U.S. Dept. of Commerce, Gaithersburg, MD

  25. Fahrni CJ, O'Halloran TV (1999) Aqueous coordination chemistry of quinoline-based fluorescence probes for the biological chemistry of zinc. J Am Chem Soc 121(49):11448–11458. https://doi.org/10.1021/Ja992709f

    Article  CAS  Google Scholar 

  26. Outten CE, O'Halloran TV (2001) Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 292(5526):2488–2492. https://doi.org/10.1126/science.1060331

    Article  CAS  PubMed  Google Scholar 

  27. Burdette SC, Walkup GK, Spingler B, Tsien RY, Lippard SJ (2001) Fluorescent sensors for Zn2+ based on a fluorescein platform: synthesis, properties and intracellular distribution. J Am Chem Soc 123(32):7831–7841. https://doi.org/10.1021/ja010059l

    Article  CAS  PubMed  Google Scholar 

  28. Zalewski PD, Forbes IJ, Betts WH (1993) Correlation of apoptosis with change in intracellular labile Zn(Ii) using zinquin [(2-methyl-8-P-toluenesulphonamido-6-quinolyloxy)acetic acid], a new specific fluorescent-probe for Zn(Ii). Biochem J 296:403–408. https://doi.org/10.1042/Bj2960403

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Chimienti F, Aouffen M, Favier A, Seve M (2003) Zinc homeostasis-regulating proteins: new drug targets for triggering cell fate. Curr Drug Targets 4(4):323–338

    Article  CAS  PubMed  Google Scholar 

  30. Thokala S, Inapurapu S, Bodiga VL, Vemuri PK, Bodiga S (2017) Loss of ErbB2-PI3K/Akt signaling prevents zinc pyrithione-induced cardioprotection during ischemia/reperfusion. Biomed Pharmacother 88:309–324. https://doi.org/10.1016/j.biopha.2017.01.065

    Article  CAS  PubMed  Google Scholar 

  31. Bodiga VL, Thokala S, Vemuri PK, Bodiga S (2015) Zinc pyrithione inhibits caspase-3 activity, promotes ErbB1-ErbB2 heterodimerization and suppresses ErbB2 downregulation in cardiomyocytes subjected to ischemia/reperfusion. J Inorg Biochem 153:49–59. https://doi.org/10.1016/j.jinorgbio.2015.09.010

    Article  CAS  PubMed  Google Scholar 

  32. Burdette SC, Walkup GK, Spingler B, Tsien RY, Lippard SJ (2001) Fluorescent sensors for Zn(2+) based on a fluorescein platform: synthesis, properties and intracellular distribution. J Am Chem Soc 123(32):7831–7841

    Article  CAS  PubMed  Google Scholar 

  33. Snitsarev V, Budde T, Stricker TP, Cox JM, Krupa DJ, Geng L, Kay AR (2001) Fluorescent detection of Zn(2+)-rich vesicles with Zinquin: mechanism of action in lipid environments. Biophys J 80(3):1538–1546. https://doi.org/10.1016/S0006-3495(01)76126-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Palmiter RD, Findley SD (1995) Cloning and functional characterization of a mammalian zinc transporter that confers resistance to zinc. EMBO J 14(4):639–649

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Palmiter RD, Cole TB, Findley SD (1996) ZnT-2, a mammalian protein that confers resistance to zinc by facilitating vesicular sequestration. EMBO J 15(8):1784–1791

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  36. Kambe T, Narita H, Yamaguchi-Iwai Y, Hirose J, Amano T, Sugiura N, Sasaki R, Mori K, Iwanaga T, Nagao M (2002) Cloning and characterization of a novel mammalian zinc transporter, zinc transporter 5, abundantly expressed in pancreatic beta cells. J Biol Chem 277(21):19049–19055. https://doi.org/10.1074/jbc.M200910200

    Article  CAS  PubMed  Google Scholar 

  37. Chen YH, Kim JH, Stallcup MR (2005) GAC63, a GRIP1-dependent nuclear receptor coactivator. Mol Cell Biol 25(14):5965–5972. https://doi.org/10.1128/MCB.25.14.5965-5972.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Dufner-Beattie J, Langmade SJ, Wang F, Eide D, Andrews GK (2003) Structure, function, and regulation of a subfamily of mouse zinc transporter genes. J Biol Chem 278(50):50142–50150. https://doi.org/10.1074/jbc.M304163200

    Article  CAS  PubMed  Google Scholar 

  39. Wang F, Dufner-Beattie J, Kim BE, Petris MJ, Andrews G, Eide DJ (2004) Zinc-stimulated endocytosis controls activity of the mouse ZIP1 and ZIP3 zinc uptake transporters. J Biol Chem 279(23):24631–24639. https://doi.org/10.1074/jbc.M400680200

    Article  CAS  PubMed  Google Scholar 

  40. Gaither LA, Eide DJ (2000) Functional expression of the human hZIP2 zinc transporter. J Biol Chem 275(8):5560–5564

    Article  CAS  PubMed  Google Scholar 

  41. Kelleher SL, Lonnerdal B (2003) Zn transporter levels and localization change throughout lactation in rat mammary gland and are regulated by Zn in mammary cells. J Nutr 133(11):3378–3385. https://doi.org/10.1093/jn/133.11.3378

    Article  CAS  PubMed  Google Scholar 

  42. Kong BY, Duncan FE, Que EL, Kim AM, O'Halloran TV, Woodruff TK (2014) Maternally-derived zinc transporters ZIP6 and ZIP10 drive the mammalian oocyte-to-egg transition. Mol Hum Reprod 20(11):1077–1089. https://doi.org/10.1093/molehr/gau066

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Lichten LA, Ryu MS, Guo L, Embury J, Cousins RJ (2011) MTF-1-mediated repression of the zinc transporter Zip10 is alleviated by zinc restriction. PLoS One 6(6):e21526. https://doi.org/10.1371/journal.pone.0021526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Girijashanker K, He L, Soleimani M, Reed JM, Li H, Liu Z, Wang B, Dalton TP, Nebert DW (2008) Slc39a14 gene encodes ZIP14, a metal/bicarbonate symporter: similarities to the ZIP8 transporter. Mol Pharmacol 73(5):1413–1423. https://doi.org/10.1124/mol.107.043588

    Article  CAS  PubMed  Google Scholar 

  45. Huang L, Kirschke CP, Zhang Y, Yu YY (2005) The ZIP7 gene (Slc39a7) encodes a zinc transporter involved in zinc homeostasis of the Golgi apparatus. J Biol Chem 280(15):15456–15463. https://doi.org/10.1074/jbc.M412188200

    Article  CAS  PubMed  Google Scholar 

  46. Grubman A, Lidgerwood GE, Duncan C, Bica L, Tan JL, Parker SJ, Caragounis A, Meyerowitz J, Volitakis I, Moujalled D, Liddell JR, Hickey JL, Horne M, Longmuir S, Koistinaho J, Donnelly PS, Crouch PJ, Tammen I, White AR, Kanninen KM (2014) Deregulation of subcellular biometal homeostasis through loss of the metal transporter, Zip7, in a childhood neurodegenerative disorder. Acta Neuropathol Commun 2:25. https://doi.org/10.1186/2051-5960-2-25

    Article  PubMed  PubMed Central  Google Scholar 

  47. Matsuura W, Yamazaki T, Yamaguchi-Iwai Y, Masuda S, Nagao M, Andrews GK, Kambe T (2009) SLC39A9 (ZIP9) regulates zinc homeostasis in the secretory pathway: characterization of the ZIP subfamily I protein in vertebrate cells. Biosci Biotechnol Biochem 73(5):1142–1148. https://doi.org/10.1271/bbb.80910

    Article  CAS  PubMed  Google Scholar 

  48. Martin AB, Aydemir TB, Guthrie GJ, Samuelson DA, Chang SM, Cousins RJ (2013) Gastric and colonic zinc transporter ZIP11 (Slc39a11) in mice responds to dietary zinc and exhibits nuclear localization. J Nutr 143(12):1882–1888. https://doi.org/10.3945/jn.113.184457

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Bin BH, Fukada T, Hosaka T, Yamasaki S, Ohashi W, Hojyo S, Miyai T, Nishida K, Yokoyama S, Hirano T (2011) Biochemical characterization of human ZIP13 protein: a homo-dimerized zinc transporter involved in the spondylocheiro dysplastic Ehlers-Danlos syndrome. J Biol Chem 286(46):40255–40265. https://doi.org/10.1074/jbc.M111.256784

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Langmade SJ, Ravindra R, Daniels PJ, Andrews GK (2000) The transcription factor MTF-1 mediates metal regulation of the mouse ZnT1 gene. J Biol Chem 275(44):34803–34809. https://doi.org/10.1074/jbc.M007339200

    Article  CAS  PubMed  Google Scholar 

  51. Itsumura N, Inamo Y, Okazaki F, Teranishi F, Narita H, Kambe T, Kodama H (2013) Compound heterozygous mutations in SLC30A2/ZnT2 results in low milk zinc concentrations: a novel mechanism for zinc deficiency in a breast-fed infant. PLoS One 8(5):e64045. https://doi.org/10.1371/journal.pone.0064045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Falcon-Perez JM, Dell'Angelica EC (2007) Zinc transporter 2 (SLC30A2) can suppress the vesicular zinc defect of adaptor protein 3-depleted fibroblasts by promoting zinc accumulation in lysosomes. Exp Cell Res 313(7):1473–1483. https://doi.org/10.1016/j.yexcr.2007.02.006

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Lopez V, Kelleher SL (2009) Zinc transporter-2 (ZnT2) variants are localized to distinct subcellular compartments and functionally transport zinc. Biochem J 422(1):43–52. https://doi.org/10.1042/BJ20081189

    Article  CAS  PubMed  Google Scholar 

  54. Guo L, Lichten LA, Ryu MS, Liuzzi JP, Wang F, Cousins RJ (2010) STAT5-glucocorticoid receptor interaction and MTF-1 regulate the expression of ZnT2 (Slc30a2) in pancreatic acinar cells. Proc Natl Acad Sci U S A 107(7):2818–2823. https://doi.org/10.1073/pnas.0914941107

    Article  PubMed  PubMed Central  Google Scholar 

  55. Suzuki T, Ishihara K, Migaki H, Ishihara K, Nagao M, Yamaguchi-Iwai Y, Kambe T (2005) Two different zinc transport complexes of cation diffusion facilitator proteins localized in the secretory pathway operate to activate alkaline phosphatases in vertebrate cells. J Biol Chem 280(35):30956–30962. https://doi.org/10.1074/jbc.M506902200

    Article  CAS  PubMed  Google Scholar 

  56. Homma K, Fujisawa T, Tsuburaya N, Yamaguchi N, Kadowaki H, Takeda K, Nishitoh H, Matsuzawa A, Naguro I, Ichijo H (2013) SOD1 as a molecular switch for initiating the homeostatic ER stress response under zinc deficiency. Mol Cell 52(1):75–86. https://doi.org/10.1016/j.molcel.2013.08.038

    Article  CAS  PubMed  Google Scholar 

  57. Ellis CD, Wang F, MacDiarmid CW, Clark S, Lyons T, Eide DJ (2004) Zinc and the Msc2 zinc transporter protein are required for endoplasmic reticulum function. J Cell Biol 166(3):325–335. https://doi.org/10.1083/jcb.200401157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Ishihara K, Yamazaki T, Ishida Y, Suzuki T, Oda K, Nagao M, Yamaguchi-Iwai Y, Kambe T (2006) Zinc transport complexes contribute to the homeostatic maintenance of secretory pathway function in vertebrate cells. J Biol Chem 281(26):17743–17750. https://doi.org/10.1074/jbc.M602470200

    Article  CAS  PubMed  Google Scholar 

  59. Coneyworth LJ, Jackson KA, Tyson J, Bosomworth HJ, van der Hagen E, Hann GM, Ogo OA, Swann DC, Mathers JC, Valentine RA, Ford D (2012) Identification of the human zinc transcriptional regulatory element (ZTRE): a palindromic protein-binding DNA sequence responsible for zinc-induced transcriptional repression. J Biol Chem 287(43):36567–36581. https://doi.org/10.1074/jbc.M112.397000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Dufner-Beattie J, Wang F, Kuo YM, Gitschier J, Eide D, Andrews GK (2003) The acrodermatitis enteropathica gene ZIP4 encodes a tissue-specific, zinc-regulated zinc transporter in mice. J Biol Chem 278(35):33474–33481. https://doi.org/10.1074/jbc.M305000200

    Article  CAS  PubMed  Google Scholar 

  61. Gaither LA, Eide DJ (2001) The human ZIP1 transporter mediates zinc uptake in human K562 erythroleukemia cells. J Biol Chem 276(25):22258–22264. https://doi.org/10.1074/jbc.M101772200

    Article  CAS  PubMed  Google Scholar 

  62. Huang L, Kirschke CP (2007) A di-leucine sorting signal in ZIP1 (SLC39A1) mediates endocytosis of the protein. FEBS J 274(15):3986–3997. https://doi.org/10.1111/j.1742-4658.2007.05933.x

    Article  PubMed  Google Scholar 

  63. Weaver BP, Dufner-Beattie J, Kambe T, Andrews GK (2007) Novel zinc-responsive post-transcriptional mechanisms reciprocally regulate expression of the mouse Slc39a4 and Slc39a5 zinc transporters (Zip4 and Zip5). Biol Chem 388(12):1301–1312. https://doi.org/10.1515/BC.2007.149

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Taylor KM, Morgan HE, Johnson A, Nicholson RI (2005) Structure-function analysis of a novel member of the LIV-1 subfamily of zinc transporters, ZIP14. FEBS Lett 579(2):427–432. https://doi.org/10.1016/j.febslet.2004.12.006

    Article  CAS  PubMed  Google Scholar 

  65. Taylor KM, Morgan HE, Johnson A, Nicholson RI (2004) Structure-function analysis of HKE4, a member of the new LIV-1 subfamily of zinc transporters. Biochem J 377(Pt 1):131–139. https://doi.org/10.1042/BJ20031183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Taylor KM, Hiscox S, Nicholson RI, Hogstrand C, Kille P (2012) Protein kinase CK2 triggers cytosolic zinc signaling pathways by phosphorylation of zinc channel ZIP7. Sci Signal 5(210):ra11. https://doi.org/10.1126/scisignal.2002585

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Taniguchi M, Fukunaka A, Hagihara M, Watanabe K, Kamino S, Kambe T, Enomoto S, Hiromura M (2013) Essential role of the zinc transporter ZIP9/SLC39A9 in regulating the activations of Akt and Erk in B-cell receptor signaling pathway in DT40 cells. PLoS One 8(3):e58022. https://doi.org/10.1371/journal.pone.0058022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Kelleher SL, Velasquez V, Croxford TP, McCormick NH, Lopez V, MacDavid J (2012) Mapping the zinc-transporting system in mammary cells: molecular analysis reveals a phenotype-dependent zinc-transporting network during lactation. J Cell Physiol 227(4):1761–1770. https://doi.org/10.1002/jcp.22900

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Yu Y, Wu A, Zhang Z, Yan G, Zhang F, Zhang L, Shen X, Hu R, Zhang Y, Zhang K, Wang F (2013) Characterization of the GufA subfamily member SLC39A11/Zip11 as a zinc transporter. J Nutr Biochem 24(10):1697–1708. https://doi.org/10.1016/j.jnutbio.2013.02.010

    Article  CAS  PubMed  Google Scholar 

  70. Jeong J, Walker JM, Wang F, Park JG, Palmer AE, Giunta C, Rohrbach M, Steinmann B, Eide DJ (2012) Promotion of vesicular zinc efflux by ZIP13 and its implications for spondylocheiro dysplastic Ehlers-Danlos syndrome. Proc Natl Acad Sci U S A 109(51):E3530–E3538. https://doi.org/10.1073/pnas.1211775110

    Article  PubMed  PubMed Central  Google Scholar 

  71. Fukada T, Civic N, Furuichi T, Shimoda S, Mishima K, Higashiyama H, Idaira Y, Asada Y, Kitamura H, Yamasaki S, Hojyo S, Nakayama M, Ohara O, Koseki H, Dos Santos HG, Bonafe L, Ha-Vinh R, Zankl A, Unger S, Kraenzlin ME, Beckmann JS, Saito I, Rivolta C, Ikegawa S, Superti-Furga A, Hirano T (2008) The zinc transporter SLC39A13/ZIP13 is required for connective tissue development; its involvement in BMP/TGF-beta signaling pathways. PLoS One 3(11):e3642. https://doi.org/10.1371/journal.pone.0003642

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Hojyo S, Fukada T, Shimoda S, Ohashi W, Bin BH, Koseki H, Hirano T (2011) The zinc transporter SLC39A14/ZIP14 controls G-protein coupled receptor-mediated signaling required for systemic growth. PLoS One 6(3):e18059. https://doi.org/10.1371/journal.pone.0018059

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Liuzzi JP, Lichten LA, Rivera S, Blanchard RK, Aydemir TB, Knutson MD, Ganz T, Cousins RJ (2005) Interleukin-6 regulates the zinc transporter Zip14 in liver and contributes to the hypozincemia of the acute-phase response. Proc Natl Acad Sci U S A 102(19):6843–6848. https://doi.org/10.1073/pnas.0502257102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Funding

This research was supported by grants from DST-SERB, Govt. of India (No. SB/YS/LS-222/2013), University Grants Commission (F. No.4-5(28)/2013(BSR) (FRP)) to SB.

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  1. Department of Biochemistry, Kakatiya University, Vidyaranyapuri, Warangal Urban, Telangana, India

    Sandhya Thokala, Madhukar Rao Kudle & Sreedhar Bodiga

  2. Department of Biochemistry and Molecular Biology, Institute of Genetics and Hospital for Genetic Diseases, Osmania University, Begumpet, Hyderabad, Telangana, India

    Vijaya Lakshmi Bodiga

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Thokala, S., Bodiga, V.L., Kudle, M.R. et al. Comparative Response of Cardiomyocyte ZIPs and ZnTs to Extracellular Zinc and TPEN. Biol Trace Elem Res 192, 297–307 (2019). https://doi.org/10.1007/s12011-019-01671-0

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