SLC30A3 (ZnT3) oligomerization by dityrosine bonds regulates its subcellular localization and metal transport capacity

PLoS ONE

Volumn 4, Issue 6, 2009, Pages

  Salazar, Gloria ^a   Falcon Perez, Juan M ^b   Harrison, Robert ^c   Faundez, Victor ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b INSTITUTO DE SALUD CARLOS III   (Spain)

^c GEORGIA STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

SOLUTE CARRIER FAMILY 30 MEMBER 3; UNCLASSIFIED DRUG; ZINC TRANSPORTER; ZINC TRANSPORTER 3; CARRIER PROTEIN; CATION TRANSPORT PROTEIN; DNA; MEMBRANE PROTEIN; METAL; SLC30A3 PROTEIN, HUMAN; SLC30A3 PROTEIN, MOUSE; TYROSINE; ZINC; ZINC TRANSPORTER 3, RAT;

ARTICLE; CELL TRANSPORT; CELLULAR DISTRIBUTION; CONTROLLED STUDY; COVALENT BOND; CROSS LINKING; DIMERIZATION; DISULFIDE BOND; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MOLECULAR WEIGHT; OLIGOMERIZATION; OXIDATIVE STRESS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN TARGETING; REGULATORY MECHANISM; SITE DIRECTED MUTAGENESIS; ANIMAL; BIOLOGICAL MODEL; CELL STRAIN; CHEMISTRY; METABOLISM; MOUSE; MUTATION; PHYSIOLOGY; RAT; TRANSPORT AT THE CELLULAR LEVEL;

ANIMALS; BIOLOGICAL TRANSPORT; CARRIER PROTEINS; CATION TRANSPORT PROTEINS; DNA; HUMANS; MEMBRANE PROTEINS; METALS; MICE; MODELS, BIOLOGICAL; MUTAGENESIS, SITE-DIRECTED; MUTATION; PC12 CELLS; RATS; TYROSINE; ZINC;

EID: 67749086712     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0005896     Document Type: Article

References (57)

1. Sitte HH, Farhan H, Javitch JA (2004) Sodium-dependent neurotransmitter transporters: oligomerization as a determinant of transporter function and trafficking. Mol Interv 4: 38-47.
2. Chen X, Molino C, Liu L, Gumbiner BM (2007) Structural elements necessary for oligomerization, trafficking, and cell sorting function of paraxial protocadherin. J Biol Chem 282: 32128-32137.
3. Pin JP, Kniazeff J, Liu J, Binet V, Goudet C, et al. (2005) Allosteric functioning of dimeric class C G-protein-coupled receptors. Febs J 272: 2947-2955.
4. Nufer O, Kappeler F, Guldbrandsen S, Hauri HP (2003) ER export of ERGIC-53 is controlled by cooperation of targeting determinants in all three of its domains. J Cell Sci 116: 4429-4440.
5. Robbins MJ, Calver AR, Filippov AK, Hirst WD, Russell RB, et al. (2001) GABA(B2) is essential for g-protein coupling of the GABA(B) receptor heterodimer. J Neurosci 21: 8043-8052.
6. Baneres JL, Parello J (2003) Structure-based analysis of GPCR function: evidence for a novel pentameric assembly between the dimeric leukotriene B4 receptor BLT1 and the G-protein. J Mol Biol 329: 815-829.
7. Funami K, Sasai M, Oshiumi H, Seya T, Matsumoto M (2008) Homo-oligomerization is essential for Toll/interleukin-1 receptor domain-containing adaptor molecule-1-mediated NF-kappaB and interferon regulatory factor-3 activation. J Biol Chem 283: 18283-18291.
8. Lemmon MA, Flanagan JM, Treutlein HR, Zhang J, Engelman DM (1992) Sequence specificity in the dimerization of transmembrane alpha-helices. Biochemistry 31: 12719-12725.
9. Senes A, Engel DE, DeGrado WF (2004) Folding of helical membrane proteins: the role of polar, GxxxG-like and proline motifs. Curr Opin Struct Biol 14: 465-479.
10. Damian M, Martin A, Mesnier D, Pin JP, Baneres JL (2006) Asymmetric conformational changes in a GPCR dimer controlled by G-proteins. Embo J 25: 5693-5702.
11. LaBella F, Keeley F, Vivian S, Thornhill D (1967) Evidence for dityrosine in elastin. Biochem Biophys Res Commun 26: 748-753.
12. Andersen SO (1964) The Cross-Links in Resilin Identified as Dityrosine and Trityrosine. Biochim Biophys Acta 93: 213-215.
13. LaBella F, Waykole P, Queen G (1968) Formation of insoluble gels and dityrosine by the action of peroxidase on soluble collagens. Biochem Biophys Res Commun 30: 333-338.
14. Edens WA, Sharling L, Cheng G, Shapira R, Kinkade JM, et al. (2001) Tyrosine cross-linking of extracellular matrix is catalyzed by Duox, a multidomain oxidase/peroxidase with homology to the phagocyte oxidase subunit gp91phox. J Cell Biol 154: 879-891.
15. Abdalla S, Lother H, El Missiry A, Sergeev P, Langer A, et al. (2008) Dominant-negative AT2 receptor oligomers induce G-protein arrest and symptoms of neurodegeneration. J Biol Chem.
16. Garcia-Castineiras S, Dillon J, Spector A (1978) Detection of bityrosine in cataractous human lens protein. Science 199: 897-899.
17. Giulivi C, Davies KJ (1994) Dityrosine: a marker for oxidatively modified proteins and selective proteolysis. Methods Enzymol 233: 363-371.
18. Hensley K, Maidt ML, Yu Z, Sang H, Markesbery WR, et al. (1998) Electrochemical analysis of protein nitrotyrosine and dityrosine in the Alzheimer brain indicates region-specific accumulation. J Neurosci 18: 8126-8132.
19. Heinecke JW (2002) Oxidized amino acids: culprits in human atherosclerosis and indicators of oxidative stress. Free Radic Biol Med 32: 1090-1101.
20. Krishnan S, Chi EY, Wood SJ, Kendrick BS, Li C, et al. (2003) Oxidative dimer formation is the critical rate-limiting step for Parkinson's disease alpha-synuclein fibrillogenesis. Biochemistry 42: 829-837.
21. Atwood CS, Perry G, Zeng H, Kato Y, Jones WD, et al. (2004) Copper mediates dityrosine cross-linking of Alzheimer's amyloid-beta. Biochemistry 43: 560-568.
22. Palmiter RD, Huang L (2004) Efflux and compartmentalization of zinc by members of the SLC30 family of solute carriers. Pflugers Arch 447: 744-751.
23. Palmiter RD, Cole TB, Quaife CJ, Findley SD (1996) ZnT-3, a putative transporter of zinc into synaptic vesicles. Proc Natl Acad Sci U S A 93: 14934-14939.
24. Cole TB, Wenzel HJ, Kafer KE, Schwartzkroin PA, Palmiter RD (1999) Elimination of zinc from synaptic vesicles in the intact mouse brain by disruption of the ZnT3 gene. Proc Natl Acad Sci U S A 96: 1716-1721.
25. Kantheti P, Qiao X, Diaz ME, Peden AA, Meyer GE, et al. (1998) Mutation in AP-3 delta in the mocha mouse links endosomal transport to storage deficiency in platelets, melanosomes, and synaptic vesicles. Neuron 21: 111-122.
26. Salazar G, Love R, Werner E, Doucette MM, Cheng S, et al. (2004) The zinc transporter ZnT3 interacts with AP-3 and it is preferentially targeted to a distinct synaptic vesicle subpopulation. Mol Biol Cell 15: 575-587.
27. Dutzler R (2004) Structural basis for ion conduction and gating in ClC chloride channels. FEBS Lett 564: 229-233.
28. Palmiter RD, Findley SD (1995) Cloning and functional characterization of a mammalian zinc transporter that confers resistance to zinc. Embo J 14: 639-649.
29. Ellis CD, Macdiarmid CW, Eide DJ (2005) Heteromeric protein complexes mediate zinc transport into the secretory pathway of eukaryotic cells. J Biol Chem 280: 28811-28818.
30. Suzuki T, Ishihara K, Migaki H, Matsuura W, Kohda A, 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: 637-643.
31. Suzuki T, Ishihara K, Migaki H, Nagao M, Yamaguchi-Iwai Y, et al. (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: 30956-30962.
32. Murgia C, Devirgiliis C, Mancini E, Donadel G, Zalewski P, et al. (2008) Diabetes-linked zinc transporter ZnT8 is a homodimeric protein expressed by distinct rodent endocrine cell types in the pancreas and other glands. Nutr Metab Cardiovasc Dis.
33. Lu M, Fu D (2007) Structure of the zinc transporter YiiP. Science 317: 1746-1748.
34. Guo J, Wenk MR, Pellegrini L, Onofri F, Benfenati F, et al. (2003) Phosphatidylinositol 4-kinase type IIalpha is responsible for the phosphatidylinositol 4-kinase activity associated with synaptic vesicles. Proc Natl Acad Sci U S A 100: 3995-4000.
35. Advani RJ, Yang B, Prekeris R, Lee KC, Klumperman J, et al. (1999) VAMP-7 mediates vesicular transport from endosomes to lysosomes. J Cell Biol 146: 765-776.
36. Salazar G, Love R, Styers ML, Werner E, Peden A, et al. (2004) AP-3-dependent mechanisms control the targeting of a chloride channel (ClC-3) in neuronal and non-neuronal cells. J Biol Chem 279: 25430-25439.
37. 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: 1473-1483.
38. Craige B, Salazar G, Faundez V (2008) Phosphatidylinositol-4-kinase type II alpha contains an AP-3-sorting motif and a kinase domain that are both required for endosome traffic. Mol Biol Cell 19: 1415-1426.
39. Clift-O'Grady L, Desnos C, Lichtenstein Y, Faundez V, Horng JT, et al. (1998) Reconstitution of synaptic vesicle biogenesis from PC12 cell membranes. Methods 16: 150-159.
40. Salazar G, Craige B, Love R, Kalman D, Faundez V (2005) Vglut1 and ZnT3 co-targeting mechanisms regulate vesicular zinc stores in PC12 cells. J Cell Sci 118: 1911-1921.
41. Harrison RW, Chatterjee D, Weber IT (1995) Analysis of six protein structures predicted by comparative modeling techniques. Proteins 23: 463-471.
42. Harrison R (1999) A self-assembling neural network for modeling polymers. J Math Chem 26: 125-137.
43. Bagossi P, Zahuczky G, J. T, I.T. W, R.W. H (1999) "Improved Parameters for Generating Partial Charges: Correlation with Observed Dipole Moments". J Mol Model 5: 143-152.
44. Harrison RW (2003) Amortized fast multipole algorithm for molecular modeling. Proceedings of the International Conference on Computer Science and its Applications, Eds, Pradip Peter Dey, Mohammad N Amin, Thomas M Gatton ICCSA. pp 77-81.
45. DeLano WL (2002) The PyMOL Molecular graphics System. San Carlos, CA, USA: DeLano Scientific.
46. Saitoh H, Hinchey J (2000) Functional heterogeneity of small ubiquitin-related protein modifiers SUMO-1 versus SUMO-2/3. J Biol Chem 275: 6252-6258.
47. Lee DH, Goldberg AL (1998) Proteasome inhibitors: valuable new tools for cell biologists. Trends Cell Biol 8: 397-403.
48. Malencik DA, Anderson SR (2003) Dityrosine as a product of oxidative stress and fluorescent probe. Amino Acids 25: 233-247.
49. Newell-Litwa KA, Salazar G, Smith Y, Faundez V (2009) Roles of BLOC1 and AP-3 complexes in cargo sorting to synaptic vesicles. Mol Biol Cell In Press.
50. Craige B, Salazar G, Faundez V (2004) Isolation of synaptic vesicles. Curr Protoc Cell Biol Chapter 3: Unit 3 12.
51. Grote E, Hao JC, Bennett MK, Kelly RB (1995) A targeting signal in VAMP regulating transport to synaptic vesicles. Cell 81: 581-589.
52. Faundez V, Horng JT, Kelly RB (1997) ADP ribosylation factor 1 is required for synaptic vesicle budding in PC12 cells. J Cell Biol 138: 505-515.
53. Schmidt A, Hannah MJ, Huttner WB (1997) Synaptic-like microvesicles of neuroendocrine cells originate from a novel compartment that is continuous with the plasma membrane and devoid of transferrin receptor. J Cell Biol 137: 445-458.
54. 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 (Pt 2): 403-408.
55. Hastrup H, Karlin A, Javitch JA (2001) Symmetrical dimer of the human dopamine transporter revealed by cross-linking Cys-306 at the extracellular end of the sixth transmembrane segment. Proc Natl Acad Sci U S A 98: 10055-10060.
56. Bartholomaus I, Milan-Lobo L, Nicke A, Dutertre S, Hastrup H, et al. (2008) Glycine transporter dimers: evidence for occurrence in the plasma membrane. J Biol Chem 283: 10978-10991.
57. Tao RH, Maruyama IN (2008) All EGF(ErbB) receptors have preformed homo-and heterodimeric structures in living cells. J Cell Sci 121: 3207-3217.