Heterodimerization, altered subcellular localization, and function of multiple zinc transporters in viable cells using bimolecular fluorescence complementation

Journal of Biological Chemistry

Volumn 290, Issue 14, 2015, Pages 9050-9063

  Golan, Yarden ^a   Berman, Bluma ^a   Assaraf, Yehuda G ^a  

^a TECHNION ISRAEL INSTITUTE OF TECHNOLOGY   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CELL MEMBRANES; FLUORESCENCE; PHYSIOLOGY;

DELETERIOUS EFFECTS; HETERODIMER FORMATION; INTRACELLULAR COMPARTMENTS; INTRACELLULAR ORGANELLE; INTRACELLULAR VESICLES; PATHOLOGICAL CONDITIONS; PHYSIOLOGICAL FUNCTIONS; SUBCELLULAR LOCALIZATIONS;

ZINC;

COMPLEMENTARY DNA; HETERODIMER; HOMODIMER; UNCLASSIFIED DRUG; ZINC TRANSPORTER; ZINC TRANSPORTER 1; ZINC TRANSPORTER 2; ZINC TRANSPORTER 3; ZINC TRANSPORTER 4; CARRIER PROTEIN; PRIMER DNA; ZINC-BINDING PROTEIN;

ARTICLE; BIMOLECULAR FLUORESCENCE COMPLEMENTATION; CELL MEMBRANE; CELL VACUOLE; CELL VIABILITY; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DIMERIZATION; FLUORESCENCE ANALYSIS; GENE MUTATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; CELL FRACTIONATION; FEMALE; FLUORESCENCE MICROSCOPY; HUMAN; MCF 7 CELL LINE; METABOLISM; NUCLEOTIDE SEQUENCE;

BASE SEQUENCE; CARRIER PROTEINS; DIMERIZATION; DNA PRIMERS; FEMALE; HUMANS; MCF-7 CELLS; MICROSCOPY, FLUORESCENCE; SUBCELLULAR FRACTIONS;

EID: 84926432112     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M114.617332     Document Type: Article

References (42)

1. Eide, D. J. (2006) Zinc transporters and the cellular trafficking of zinc. Biochim. Biophys. Acta 1763, 711-722
2. Palmiter, R. D., and Huang, L. (2004) Efflux and compartmentalization of zinc by members of the SLC30 family of solute carriers. Pflugers Arch. 447, 744-751
3. Wessells, K. R., and Brown, K. H. (2012) Estimating the global prevalence of zinc deficiency: results based on zinc availability in national food supplies and the prevalence of stunting. PLoS One 7, e50568
4. Prasad, A. S. (2012) Discovery of human zinc deficiency: 50 years later. J. Trace Elem. Med. Biol. 26, 66-69
5. Lee, J., Yim, Y. S., Ko, S. J., Kim, D. G., and Kim, C. H. (2011) Gap junctions contribute to astrocytic resistance against zinc toxicity. Brain Res. Bull. 86, 314-318
6. Huang, L., and Tepaamorndech, S. (2013) The SLC30 family of zinc transporters: a review of current understanding of their biological and pathophysiological roles. Mol. Aspects Med. 34, 548-560
7. Jeong, J., and Eide, D. J. (2013) The SLC39 family of zinc transporters. Mol. Aspects Med. 34, 612-619
8. Chowanadisai, W., Lönnerdal, B., and Kelleher, S. L. (2006) Identification of a mutation in SLC30A2 (ZnT-2) in women with low milk zinc concentration that results in transient neonatal zinc deficiency. J. Biol. Chem. 281, 39699-39707
9. Itsumura, N., Inamo, Y., Okazaki, F., Teranishi, F., Narita, H., Kambe, T., and 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, e64045
10. Krieger, I., Alpern, B. E., and Cunnane, S. C. (1986) Transient neonatal zinc deficiency. Am. J. Clin. Nutr. 43, 955-958
11. Lasry, I., Seo, Y. A., Ityel, H., Shalva, N., Pode-Shakked, B., Glaser, F., Berman, B., Berezovsky, I., Goncearenco, A., Klar, A., Levy, J., Anikster, Y., Kelleher, S. L., and Assaraf, Y. G. (2012) A dominant negative heterozygous G87R mutation in the zinc transporter, ZnT-2 (SLC30A2), results in transient neonatal zinc deficiency. J. Biol. Chem. 287, 29348-29361
12. Lova Navarro, M., Vera Casaño, A., Benito Lopez, C., Fernández Ballesteros, M. D., Godoy Diáz, D. J., Crespo Erchiga, A., and Romero Brufau, S. (2014) Transient neonatal zinc deficiency due to a new autosomal dominant mutation in gene SLC30A2 (ZnT-2). Pediatr. Dermatol. 31, 251-252
13. Miletta, M. C., Bieri, A., Kernland, K., Schöni, M. H., Petkovic, V., Flück, C. E., Eblé, A., and Mullis, P. E. (2013) Transient neonatal zinc deficiency caused by a heterozygous G87R mutation in the zinc transporter ZnT-2 (SLC30A2) gene in the mother highlighting the importance of Zn2+ for normal growth and development. Int. J. Endocrinol. 2013, 259189
14. Adlard, P. A., Parncutt, J. M., Finkelstein, D. I., and Bush, A. I. (2010) Cognitive loss in zinc transporter-3 knock-out mice: a phenocopy for the synaptic and memory deficits of Alzheimer's disease? J. Neurosci. 30, 1631-1636
15. Weijers, R. N. (2010) Three-dimensional structure of β-cell-specific zinc transporter, ZnT-8, predicted from the type 2 diabetes-associated gene variant SLC30A8 R325W. Diabetol Metab. Syndr. 2, 33
16. Gohlke, H., Ferrari, U., Koczwara, K., Bonifacio, E., Illig, T., and Ziegler, A. G. (2008) SLC30A8 (ZnT8) Polymorphism is associated with young age at type 1 diabetes onset. Rev. Diabet. Stud. 5, 25-27
17. Coudray, N., Valvo, S., Hu, M., Lasala, R., Kim, C., Vink, M., Zhou, M., Provasi, D., Filizola, M., Tao, J., Fang, J., Penczek, P. A., Ubarretxena-Belandia, I., and Stokes, D. L. (2013) Inward-facing conformation of the zinc transporter YiiP revealed by cryoelectron microscopy. Proc. Natl. Acad. Sci. U.S.A. 110, 2140-2145
18. Lu, M., and Fu, D. (2007) Structure of the zinc transporter YiiP. Science 317, 1746-1748
19. Lu, M., Chai, J., and Fu, D. (2009) Structural basis for autoregulation of the zinc transporter YiiP. Nat. Struct. Mol. Biol. 16, 1063-1067
20. Salazar, G., Falcon-Perez, J. M., Harrison, R., and Faundez, V. (2009) SLC30A3 (ZnT3) oligomerization by dityrosine bonds regulates its subcellular localization and metal transport capacity. PLoS One 4, e5896
21. Fukunaka, A., Suzuki, T., Kurokawa, Y., Yamazaki, T., Fujiwara, N., Ishihara, K., Migaki, H., Okumura, K., Masuda, S., Yamaguchi-Iwai, Y., Nagao, M., and Kambe, T. (2009) Demonstration and characterization of the heterodimerization of ZnT5 and ZnT6 in the early secretory pathway. J. Biol. Chem. 284, 30798-30806
22. Lasry, I., Golan, Y., Berman, B., Amram, N., Glaser, F., and Assaraf, Y. G. (2014) In situ dimerization of multiple wild type and mutant zinc transporters in live cells using bimolecular fluorescence complementation. J. Biol. Chem. 289, 7275-7292
23. Hu, C. D., Chinenov, Y., and Kerppola, T. K. (2002) Visualization of interactions among bZIP and Rel family proteins in living cells using bimolecular fluorescence complementation. Mol. Cell 9, 789-798
24. Kerppola, T. K. (2006) Design and implementation of bimolecular fluorescence complementation (BiFC) assays for the visualization of protein interactions in living cells. Nat. Protoc. 1, 1278-1286
25. Falcón-Pérez, J. M., and Dell'Angelica, E. C. (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
26. Kukic, I., Kelleher, S. L., and Kiselyov, K. (2014) Zinc efflux through lysosomal exocytosis prevents zinc-induced toxicity. J. Cell Sci. 127, 3094-3103
27. Seo, Y. A., and Kelleher, S. L. (2010) Functional analysis of two single nucleotide polymorphisms in SLC30A2 (ZnT2): implications for mammary gland function and breast disease in women. Physiol. Genomics 42A, 219-227
28. Lopez, V., and Kelleher, S. L. (2009) Zinc transporter-2 (ZnT2) variants are localized to distinct subcellular compartments and functionally transport zinc. Biochem. J. 422, 43-52
29. Seo, Y. A., Lopez, V., and Kelleher, S. L. (2011) A histidine-rich motif mediates mitochondrial localization of ZnT2 to modulate mitochondrial function. Am. J. Physiol. Cell Physiol. 300, C1479-C1489
30. Kerppola, T. K. (2009) Visualization of molecular interactions using bimolecular fluorescence complementation analysis: characteristics of protein fragment complementation. Chem. Soc. Rev. 38, 2876-2886
31. Lee, A. S. (2005) The ER chaperone and signaling regulator GRP78/BiP as a monitor of endoplasmic reticulum stress. Methods 35, 373-381
32. Lazarczyk, M., Cassonnet, P., Pons, C., Jacob, Y., and Favre, M. (2009) The EVER proteins as a natural barrier against papillomaviruses: a new insight into the pathogenesis of human papillomavirus infections. Microbiol. Mol. Biol. Rev. 73, 348-370
33. Kambe, T., Hashimoto, A., and Fujimoto, S. (2014) Current understanding of ZIP and ZnT zinc transporters in human health and diseases. Cell. Mol. Life Sci. 71, 3281-3295
34. Nolte, C., Gore, A., Sekler, I., Kresse, W., Hershfinkel, M., Hoffmann, A., Kettenmann, H., and Moran, A. (2004) ZnT-1 expression in astroglial cells protects against zinc toxicity and slows the accumulation of intracellular zinc. Glia 48, 145-155
35. Michalczyk, A. A., Allen, J., Blomeley, R. C., and Ackland, M. L. (2002) Constitutive expression of hZnT4 zinc transporter in human breast epithelial cells. Biochem. J. 364, 105-113
36. Overbeck, S., Uciechowski, P., Ackland, M. L., Ford, D., and Rink, L. (2008) Intracellular zinc homeostasis in leukocyte subsets is regulated by different expression of zinc exporters ZnT-1 to ZnT-9. J. Leukoc. Biol. 83, 368-380
37. Haider, A. J., Briggs, D., Self, T. J., Chilvers, H. L., Holliday, N. D., and Kerr, I. D. (2011) Dimerization of ABCG2 analysed by bimolecular fluorescence complementation. PLoS One 6, e25818
38. Susperreguy, S., Prendes, L. P., Desbats, M. A., Charó, N. L., Brown, K., MacDougald, O. A., Kerppola, T., Schwartz, J., and Piwien-Pilipuk, G. (2011) Visualization by BiFC of different C/EBPβ dimers and their interaction with HP1α reveals a differential subnuclear distribution of complexes in living cells. Exp. Cell Res. 317, 706-723
39. Kilpatrick, L. E., and Holliday, N. D. (2012) Dissecting the pharmacology of G protein-coupled receptor signaling complexes using bimolecular fluorescence complementation. Methods Mol. Biol. 897, 109-138
40. Vaniotis, G., Allen, B. G., and Hébert, T. E. (2011) Nuclear GPCRs in cardiomyocytes: an insider's view of β-adrenergic receptor signaling. Am. J. Physiol. Heart Circ. Physiol. 301, H1754-H1764
41. Qian, L., Lopez, V., Seo, Y. A., and Kelleher, S. L. (2009) Prolactin regulates ZNT2 expression through the JAK2/STAT5 signaling pathway in mammary cells. Am. J. Physiol. Cell Physiol. 297, C369-C377
42. Beyer, N., Coulson, D. T., Heggarty, S., Ravid, R., Irvine, G. B., Hellemans, J., and Johnston, J. A. (2009) ZnT3 mRNA levels are reduced in Alzheimer's disease post-mortem brain. Mol. Neurodegener. 4, 53