Promotion of vesicular zinc efflux by ZIP13 and its implications for spondylocheiro dysplastic Ehlers-Danlos syndrome

Proceedings of the National Academy of Sciences of the United States of America

Volumn 109, Issue 51, 2012, Pages

  Jeong, Jeeyon ^a   Walker, Joel M ^a,d   Wang, Fudi ^c,e   Park, J Genevieve ^b   Palmer, Amy E ^b   Giunta, Cecilia ^c   Rohrbach, Marianne ^c   Steinmann, Beat ^c   Eide, David J ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b UNIVERSITY OF COLORADO   (United States)

^c UNIVERSITY CHILDREN S HOSPITAL   (Switzerland)

^d UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^e Chinese Academy of Sciences   (China)

Author keywords

Collagen; Homeostasis

Indexed keywords

LYSINE; PROLINE; PROTEIN ZIP 13; UNCLASSIFIED DRUG; ZINC; ZINC TRANSPORTER;

ARTICLE; CELL MEMBRANE; CELL VACUOLE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; EHLERS DANLOS SYNDROME; ENDOPLASMIC RETICULUM; HUMAN; HUMAN CELL; HYDROXYLATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; SPONDYLOCHEIRO DYSPLASTIC FORM OF EHLERS DANLOS SYNDROME; ZINC DEFICIENCY;

BIOLOGICAL TRANSPORT; CATION TRANSPORT PROTEINS; CYTOSOL; EHLERS-DANLOS SYNDROME; ENDOPLASMIC RETICULUM; FIBROBLASTS; HEK293 CELLS; HELA CELLS; HUMANS; MICROSCOPY, FLUORESCENCE; MODELS, GENETIC; MUTATION; RNA, SMALL INTERFERING; TISSUE DISTRIBUTION; ZINC;

MAMMALIA;

EID: 84871396523     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1211775110     Document Type: Article

References (56)

1. Vinkenborg JL, et al. (2009) Genetically encoded FRET sensors to monitor intracellular Zn2+ homeostasis. Nat Methods 6(10):737-740.
2. 2+ with genetically encoded sensors. Proc Natl Acad Sci USA 108(18):7351-7356.
3. Lichten LA, Cousins RJ (2009) Mammalian zinc transporters: Nutritional and physiologic regulation. Annu Rev Nutr 29:153-176.
4. Leach MR, Cohen-Doyle MF, Thomas DY, Williams DB (2002) Localization of the lectin, ERp57 binding, and polypeptide binding sites of calnexin and calreticulin. J Biol Chem 277(33):29686-29697.
5. Sevlever D, Mann KJ, Medof ME (2001) Differential effect of 1,10-phenanthroline on mammalian, yeast, and parasite glycosylphosphatidylinositol anchor synthesis. Biochem Biophys Res Commun 288(5):1112-1118.
6. Mann KJ, Sevlever D (2001) 1,10-Phenanthroline inhibits glycosylphosphatidylinositol anchoring by preventing phosphoethanolamine addition to glycosylphosphatidylinositol anchor precursors. Biochemistry 40(5):1205-1213.
7. Chang C, Werb Z (2001) The many faces of metalloproteases: Cell growth, invasion, angiogenesis and metastasis. Trends Cell Biol 11(11):S37-S43.
8. Zurutuza L, et al. (1999) Correlations of genotype and phenotype in hypophosphatasia. Hum Mol Genet 8(6):1039-1046.
9. Turner AJ, Hooper NM (2002) The angiotensin-converting enzyme gene family: Genomics and pharmacology. Trends Pharmacol Sci 23(4):177-183.
10. Ellis CD, et al. (2004) Zinc and the Msc2 zinc transporter protein are required for endoplasmic reticulum function. J Cell Biol 166(3):325-335.
11. Suzuki T, et al. (2005) Zinc transporters, ZnT5 and ZnT7, are required for the activation of alkaline phosphatases, zinc-requiring enzymes that are glycosylphosphatidylinositol-anchored to the cytoplasmic membrane. J Biol Chem 280(1):637-643.
12. Chimienti F, et al. (2006) In vivo expression and functional characterization of the zinc transporter ZnT8 in glucose-induced insulin secretion. J Cell Sci 119(Pt 20):4199-4206.
13. 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.
14. Matsuura W, et al. (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.
15. Jeong J, Eide D (2012) The SLC39 family of zinc transporters. Mol Asp Med, in press.
16. Giunta C, et al. (2008) Spondylocheiro dysplastic form of the Ehlers-Danlos syndrome - an autosomal-recessive entity caused by mutations in the zinc transporter gene SLC39A13. Am J Hum Genet 82(6):1290-1305.
17. Fukada T, et al. (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.
18. Steinmann B, Royce PM, Superti-Furga A (2002) The Ehlers-Danols syndrome. Connective tissue and its heritable disorders, eds Royce PM, Steinmann B (Wiley-Liss, New York), pp 431-523.
19. Yeowell HN, Walker LC (2000) Mutations in the lysyl hydroxylase 1 gene that result in enzyme deficiency and the clinical phenotype of Ehlers-Danlos syndrome type VI. Mol Genet Metab 71(1-2):212-224.
20. Franklin RB, et al. (2003) Human ZIP1 is a major zinc uptake transporter for the accumulation of zinc in prostate cells. J Inorg Biochem 96(2-3):435-442.
21. Gaither LA, Eide DJ (2001) The human ZIP1 transporter mediates zinc uptake in human K562 erythroleukemia cells. J Biol Chem 276(25):22258-22264.
22. Wang F, Kim BE, Petris MJ, Eide DJ (2004) The mammalian Zip5 protein is a zinc transporter that localizes to the basolateral surface of polarized cells. J Biol Chem 279(49):51433-51441.
23. 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.
24. Rath A, Glibowicka M, Nadeau VG, Chen G, Deber CM (2009) Detergent binding explains anomalous SDS-PAGE migration of membrane proteins. Proc Natl Acad Sci USA 106(6):1760-1765.
25. Bin BH, et al. (2011) Biochemical characterization of human ZIP13 protein: A homodimerized zinc transporter involved in the spondylocheiro dysplastic Ehlers-Danlos syndrome. J Biol Chem 286(46):40255-40265.
26. Haase H, Beyersmann D (1999) Uptake and intracellular distribution of labile and total Zn(II) in C6 rat glioma cells investigated with fl uorescent probes and atomic absorption. Biometals 12(3):247-254.
27. 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.
28. Andrews GK (2001) Cellular zinc sensors: MTF-1 regulation of gene expression. Biometals 14(3-4):223-237.
29. Bittel D, Dalton T, Samson SL, Gedamu L, Andrews GK (1998) The DNA binding activity of metal response element-binding transcription factor-1 is activated in vivo and in vitro by zinc, but not by other transition metals. J Biol Chem 273(12):7127-7133.
30. Zhao H, Eide DJ (1997) Zap1p, a metalloregulatory protein involved in zinc-responsive transcriptional regulation in Saccharomyces cerevisiae. Mol Cell Biol 17(9):5044-5052.
31. Bird A, et al. (2000) Mapping the DNA binding domain of the Zap1 zinc-responsive transcriptional activator. J Biol Chem 275(21):16160-16166.
32. Wang Y, et al. (2000) Activation of ATF6 and an ATF6 DNA binding site by the endoplasmic reticulum stress response. J Biol Chem 275(35):27013-27020.
33. Kirschke CP, Huang L (2003) ZnT7, a novel mammalian zinc transporter, accumulates zinc in the Golgi apparatus. J Biol Chem 278(6):4096-4102.
34. LeFurgey A, Shelburne JD, Ingram P (1999) Preparatory techniques, including cryotechnology. Biomedical applications of microprobe analysis, eds Ingram P, Shelburne J, Roggli V, LeFurgey A (Academic, London), pp 59-85.
35. Lamandé SR, Bateman JF (1999) Procollagen folding and assembly: The role of endoplasmic reticulum enzymes and molecular chaperones. Semin Cell Dev Biol 10(5):455-464.
36. Van Duyn Graham L, Sweetwyne MT, Pallero MA, Murphy-Ullrich JE (2010) Intracellular calreticulin regulates multiple steps in fibrillar collagen expression, trafficking, and processing into the extracellular matrix. J Biol Chem 285(10):7067-7078.
37. Hayes S, Chawla A, Corvera S (2002) TGF beta receptor internalization into EEA1-enriched early endosomes: Role in signaling to Smad2. J Cell Biol 158(7):1239-1249.
38. Golub MS, et al. (1996) Adolescent growth and maturation in zinc-deprived rhesus monkeys [see comment]. Am J Clin Nutr 64(3):274-282.
39. Leek JC, et al. (1988) Long-term marginal zinc deprivation in rhesus monkeys. IV. Effects on skeletal growth and mineralization. Am J Clin Nutr 47(5):889-895.
40. Li Y, Yu ZL (2002) Effect of zinc on bone metabolism in fetal mouse limb culture. Biomed Environ Sci 15(4):323-329.
41. Kim JT, et al. (2009) Zinc-deficient diet decreases fetal long bone growth through decreased bone matrix formation in mice. J Med Food 12(1):118-123.
42. MacDiarmid CW, Gaither LA, Eide D (2000) Zinc transporters that regulate vacuolar zinc storage in Saccharomyces cerevisiae. EMBO J 19(12):2845-2855.
43. Ma JF, Ueno D, Zhao FJ, McGrath SP (2005) Subcellular localisation of Cd and Zn in the leaves of a Cd-hyperaccumulating ecotype of Thlaspi caerulescens. Planta 220(5):731-736.
44. Roh HC, Collier S, Guthrie J, Robertson JD, Kornfeld K (2012) Lysosome-related organelles in intestinal cells are a zinc storage site in C. elegans. Cell Metab 15(1):88-99.
45. Coyle P, et al. (1994) Measurement of zinc in hepatocytes by using a fluorescent probe, zinquin: Relationship to metallothionein and intracellular zinc. Biochem J 303(Pt 3):781-786.
46. Nasir MS, et al. (1999) The chemical cell biology of zinc: Structure and intracellular fluorescence of a zinc-quinolinesulfonamide complex. J Biol Inorg Chem 4(6):775-783.
47. Ho LH, Ratnaike RN, Zalewski PD (2000) Involvement of intracellular labile zinc in suppression of DEVD-caspase activity in human neuroblastoma cells. Biochem Biophys Res Commun 268(1):148-154.
48. Burdette SC, Walkup GK, Spingler B, Tsien RY, Lippard SJ (2001) Fluorescent sensors for Zn(2+) based on a fl uorescein platform: Synthesis, properties and intracellular distribution. J Am Chem Soc 123(32):7831-7841.
49. St Croix CM, et al. (2002) Nitric oxide-induced changes in intracellular zinc homeostasis are mediated by metallothionein/thionein. Am J Physiol Lung Cell Mol Physiol 282(2):L185-L192.
50. Michalczyk AA, Allen J, Blomeley RC, Ackland ML (2002) Constitutive expression of hZnT4 zinc transporter in human breast epithelial cells. Biochem J 364(Pt 1):105-113.
51. Haase H, Beyersmann D (2002) Intracellular zinc distribution and transport in C6 rat glioma cells. Biochem Biophys Res Commun 296(4):923-928.
52. Kobayashi T, et al. (1999) Late endosomal membranes rich in lysobisphosphatidic acid regulate cholesterol transport. Nat Cell Biol 1(2):113-118.
53. Falcón-Pérez 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.
54. 2+ in rat hepatocytes. J Pharmacol Toxicol Methods 38(4):181-187.
55. Smith PJ, et al. (2002) DNA damage-induced [Zn(2+)](i) transients: Correlation with cell cycle arrest and apoptosis in lymphoma cells. Am J Physiol Cell Physiol 283(2):C609-C622.
56. Duffy JY, et al. (2001) A decrease in intracellular zinc level precedes the detection of early indicators of apoptosis in HL-60 cells. Apoptosis 6(3):161-172.