The zinc transporter SLC39A14/ZIP14 controls G-protein coupled receptor-mediated signaling required for systemic growth

PLoS ONE

Volumn 6, Issue 3, 2011, Pages

  Hojyo, Shintaro ^a,b   Fukada, Toshiyuki ^a,b   Shimoda, Shinji ^c   Ohashi, Wakana ^a   Bin, Bum Ho ^a,d   Koseki, Haruhiko ^a   Hirano, Toshio ^a,d  

^a RIKEN Center for Integrative Medical Sciences   (Japan)

^b OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c TSURUMI UNIVERSITY   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; G PROTEIN COUPLED RECEPTOR; PARATHYROID HORMONE RECEPTOR 1; PHOSPHODIESTERASE; UNCLASSIFIED DRUG; ZINC TRANSPORTER; ZINC TRANSPORTER SLC39A14; CATION TRANSPORT PROTEIN; CYCLIC AMP; SLC39A14 PROTEIN, MOUSE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE DISEASE; CARTILAGE CELL; CELL MEMBRANE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DWARFISM; EMBRYO; ENZYME ACTIVITY; GLUCONEOGENESIS; GROWTH INHIBITION; GROWTH PLATE; GROWTH RETARDATION; HYPOPHYSIS; KNOCKOUT MOUSE; LIVER; MOUSE; NONHUMAN; OSTEOPENIA; PROTEIN SYNTHESIS REGULATION; SCOLIOSIS; SIGNAL TRANSDUCTION; TORTICOLLIS; ANIMAL; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOUSE MUTANT; PHYSIOLOGY;

MAMMALIA; MUS;

ANIMALS; CATION TRANSPORT PROTEINS; CYCLIC AMP; GROWTH PLATE; LIVER; MICE; MICE, KNOCKOUT; PITUITARY GLAND; RECEPTORS, G-PROTEIN-COUPLED; SIGNAL TRANSDUCTION;

EID: 79952977920     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0018059     Document Type: Article

References (60)

1. Prasad AS, (1995) Zinc: an overview. Nutrition 11: 93-99.
2. Vallee BL, Auld DS, (1993) New perspective on zinc biochemistry: cocatalytic sites in multi-zinc enzymes. Biochemistry 32: 6493-6500.
3. Kambe T, Weaver BP, Andrews GK, (2008) The genetics of essential metal homeostasis during development. Genesis 46: 214-228.
4. Lichten LA, Cousins RJ, (2009) Mammalian zinc transporters: nutritional and physiologic regulation. Annu Rev Nutr 29: 153-176.
5. Vallee BL, (1995) The function of metallothionein. Neurochem Int 27: 23-33.
6. Kury S, Dreno B, Bezieau S, Giraudet S, Kharfi M, et al. (2002) Identification of SLC39A4, a gene involved in acrodermatitis enteropathica. Nat Genet 31: 239-240.
7. Wang F, Kim BE, Dufner-Beattie J, Petris MJ, Andrews G, et al. (2004) Acrodermatitis enteropathica mutations affect transport activity, localization and zinc-responsive trafficking of the mouse ZIP4 zinc transporter. Hum Mol Genet 13: 563-571.
8. Fukada T, Civic N, Furuichi T, Shimoda S, Mishima K, et al. (2008) The zinc transporter SLC39A13/ZIP13 is required for connective tissue development; its involvement in BMP/TGF-β signaling pathways. PLoS One 3: e3642.
9. Bruinsma JJ, Jirakulaporn T, Muslin AJ, Kornfeld K, (2002) Zinc ions and cation diffusion facilitator proteins regulate Ras-mediated signaling. Dev Cell 2: 567-578.
10. Hogstrand C, Kille P, Nicholson RI, Taylor KM, (2009) Zinc transporters and cancer: a potential role for ZIP7 as a hub for tyrosine kinase activation. Trends Mol Med 15: 101-111.
11. Kitamura H, Morikawa H, Kamon H, Iguchi M, Hojyo S, et al. (2006) Toll-like receptor-mediated regulation of zinc homeostasis influences dendritic cell function. Nat Immunol 7: 971-977.
12. Nishida K, Hasegawa A, Nakae S, Oboki K, Saito H, et al. (2009) Zinc transporter Znt5/Slc30a5 is required for the mast cell-mediated delayed-type allergic reaction but not the immediate-type reaction. J Exp Med 206: 1351-1364.
13. Yamashita S, Miyagi C, Fukada T, Kagara N, Che YS, et al. (2004) Zinc transporter LIVI controls epithelial-mesenchymal transition in zebrafish gastrula organizer. Nature 429: 298-302.
14. Sensi SL, Paoletti P, Bush AI, Sekler I, (2009) Zinc in the physiology and pathology of the CNS. Nat Rev Neurosci 10: 780-791.
15. Besser L, Chorin E, Sekler I, Silverman WF, Atkin S, et al. (2009) Synaptically released zinc triggers metabotropic signaling via a zinc-sensing receptor in the hippocampus. J Neurosci 29: 2890-2901.
16. Hirano T, Murakami M, Fukada T, Nishida K, Yamasaki S, et al. (2008) Roles of zinc and zinc signaling in immunity: zinc as an intracellular signaling molecule. Adv Immunol 97: 149-176.
17. Yamasaki S, Sakata-Sogawa K, Hasegawa A, Suzuki T, Kabu K, et al. (2007) Zinc is a novel intracellular second messenger. J Cell Biol 177: 637-645.
18. Nilsson O, Marino R, De Luca F, Phillip M, Baron J, (2005) Endocrine regulation of the growth plate. Horm Res 64: 157-165.
19. Procter AM, Phillips JA 3rd, Cooper DN, (1998) The molecular genetics of growth hormone deficiency. Hum Genet 103: 255-272.
20. MacDonald RS, (2000) The role of zinc in growth and cell proliferation. J Nutr 130: 1500S-1508S.
21. Kronenberg HM, (2003) Developmental regulation of the growth plate. Nature 423: 332-336.
22. Ohlsson C, Bengtsson BA, Isaksson OG, Andreassen TT, Slootweg MC, (1998) Growth hormone and bone. Endocr Rev 19: 55-79.
23. Sladek R, Rocheleau G, Rung J, Dina C, Shen L, et al. (2007) A genome-wide association study identifies novel risk loci for type 2 diabetes. Nature 445: 881-885.
24. Rossi L, Migliaccio S, Corsi A, Marzia M, Bianco P, et al. (2001) Reduced growth and skeletal changes in zinc-deficient growing rats are due to impaired growth plate activity and inanition. J Nutr 131: 1142-1146.
25. Liuzzi JP, Lichten LA, Rivera S, Blanchard RK, Aydemir TB, et al. (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: 6843-6848.
26. 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: 427-432.
27. Mayo KE, Godfrey PA, Suhr ST, Kulik DJ, Rahal JO, (1995) Growth hormone-releasing hormone: synthesis and signaling. Recent Prog Horm Res 50: 35-73.
28. 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: 15456-15463.
29. 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: 131-139.
30. Gaither LA, Eide DJ, (2001) The human ZIP1 transporter mediates zinc uptake in human K562 erythroleukemia cells. J Biol Chem 276: 22258-22264.
31. Kasper G, Weiser AA, Rump A, Sparbier K, Dahl E, et al. (2005) Expression levels of the putative zinc transporter LIV-1 are associated with a better outcome of breast cancer patients. Int J Cancer 117: 961-973.
32. Milon B, Dhermy D, Pountney D, Bourgeois M, Beaumont C, (2001) Differential subcellular localization of hZip1 in adherent and non-adherent cells. FEBS Lett 507: 241-246.
33. Taylor KM, Morgan HE, Johnson A, Hadley LJ, Nicholson RI, (2003) Structure-function analysis of LIV-1, the breast cancer-associated protein that belongs to a new subfamily of zinc transporters. Biochem J 375: 51-59.
34. Dufner-Beattie J, Huang ZL, Geiser J, Xu W, Andrews GK, (2006) Mouse ZIP1 and ZIP3 genes together are essential for adaptation to dietary zinc deficiency during pregnancy. Genesis 44: 239-251.
35. Girijashanker K, He L, Soleimani M, Reed JM, Li H, et al. (2008) Slc39a14 gene encodes ZIP14, a metal/bicarbonate symporter: similarities to the ZIP8 transporter. Mol Pharmacol 73: 1413-1423.
36. Taylor KM, Nicholson RI, (2003) The LZT proteins; the LIV-1 subfamily of zinc transporters. Biochim Biophys Acta 1611: 16-30.
37. Kronenberg HM, (2006) PTHrP and skeletal development. Ann N Y Acad Sci 1068: 1-13.
38. Chung UI, Lanske B, Lee K, Li E, Kronenberg H, (1998) The parathyroid hormone/parathyroid hormone-related peptide receptor coordinates endochondral bone development by directly controlling chondrocyte differentiation. Proc Natl Acad Sci U S A 95: 13030-13035.
39. Kobayashi T, Chung UI, Schipani E, Starbuck M, Karsenty G, et al. (2002) PTHrP and Indian hedgehog control differentiation of growth plate chondrocytes at multiple steps. Development 129: 2977-2986.
40. Guo J, Iida-Klein A, Huang X, Abou-Samra AB, Segre GV, et al. (1995) Parathyroid hormone (PTH)/PTH-related peptide receptor density modulates activation of phospholipase C and phosphate transport by PTH in LLC-PK1 cells. Endocrinology 136: 3884-3891.
41. Ionescu AM, Schwarz EM, Vinson C, Puzas JE, Rosier R, et al. (2001) PTHrP modulates chondrocyte differentiation through AP-1 and CREB signaling. J Biol Chem 276: 11639-11647.
42. Conti M, Beavo J, (2007) Biochemistry and physiology of cyclic nucleotide phosphodiesterases: essential components in cyclic nucleotide signaling. Annu Rev Biochem 76: 481-511.
43. Struthers RS, Vale WW, Arias C, Sawchenko PE, Montminy MR, (1991) Somatotroph hypoplasia and dwarfism in transgenic mice expressing a non-phosphorylatable CREB mutant. Nature 350: 622-624.
44. Sakharova AA, Horowitz JF, Surya S, Goldenberg N, Harber MP, et al. (2008) Role of growth hormone in regulating lipolysis, proteolysis, and hepatic glucose production during fasting. J Clin Endocrinol Metab 93: 2755-2759.
45. Pollak M, (2008) Insulin and insulin-like growth factor signalling in neoplasia. Nat Rev Cancer 8: 915-928.
46. Herzig S, Long F, Jhala US, Hedrick S, Quinn R, et al. (2001) CREB regulates hepatic gluconeogenesis through the coactivator PGC-1. Nature 413: 179-183.
47. Andrews GK, (2000) Regulation of metallothionein gene expression by oxidative stress and metal ions. Biochem Pharmacol 59: 95-104.
48. Yoshida E, Noshiro M, Kawamoto T, Tsutsumi S, Kuruta Y, et al. (2001) Direct inhibition of Indian hedgehog expression by parathyroid hormone (PTH)/PTH-related peptide and up-regulation by retinoic acid in growth plate chondrocyte cultures. Exp Cell Res 265: 64-72.
49. St-Jacques B, Hammerschmidt M, McMahon AP, (1999) Indian hedgehog signaling regulates proliferation and differentiation of chondrocytes and is essential for bone formation. Genes Dev 13: 2072-2086.
50. Georgiev P, Okkenhaug H, Drews A, Wright D, Lambert S, et al. (2010) TRPM channels mediate zinc homeostasis and cellular growth during Drosophila larval development. Cell Metab 12: 386-397.
51. Zhou Y, Xu BC, Maheshwari HG, He L, Reed M, et al. (1997) A mammalian model for Laron syndrome produced by targeted disruption of the mouse growth hormone receptor/binding protein gene (the Laron mouse). Proc Natl Acad Sci U S A 94: 13215-13220.
52. Wang J, Zhou J, Bondy CA, (1999) Igf1 promotes longitudinal bone growth by insulin-like actions augmenting chondrocyte hypertrophy. FASEB J 13: 1985-1990.
53. Baker J, Liu JP, Robertson EJ, Efstratiadis A, (1993) Role of insulin-like growth factors in embryonic and postnatal growth. Cell 75: 73-82.
54. Anderson GJ, Frazer DM, (2005) Hepatic iron metabolism. Semin Liver Dis 25: 420-432.
55. Cousins RJ, (1996) Zinc. Present knowledge in Nutrition, eds In: Filer L. J. and, Ziegler E,E., editors. (Int Life Sci Inst Nutr Foundation, Washington, DC) pp. 293-306.
56. Percival MD, Yeh B, Falgueyret JP, (1997) Zinc dependent activation of cAMP-specific phosphodiesterase (PDE4A). Biochem Biophys Res Commun 241: 175-180.
57. von Bulow V, Rink L, Haase H, (2005) Zinc-mediated inhibition of cyclic nucleotide phosphodiesterase activity and expression suppresses TNF-α and IL-1β production in monocytes by elevation of guanosine 3′,5′-cyclic monophosphate. J Immunol 175: 4697-4705.
58. 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.
59. Ovesen J, Danscher G, Thomsen JS, Mosekilde L, Moller-Madsen B, (2004) Autometallographic tracing of zinc ions in growing bone. J Musculoskelet Neuronal Interact 4: 428-435.
60. Joyner AL, (2000) Gene targeting: a practical approach. Oxford Oxford University Press. pp. xviii, 293.