Histidine pairing at the metal transport site of mammalian ZnT transporters controls Zn2+ over Cd2+ selectivity

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

Volumn 109, Issue 19, 2012, Pages 7202-7207

  Hoch, Eitan ^a   Lin, Wei ^b   Chai, Jin ^b   Hershfinkel, Michal ^a   Fu, Dax ^b   Sekler, Israel ^a  

^a BEN GURION UNIVERSITY OF THE NEGEV   (Israel)

^b BROOKHAVEN NATIONAL LABORATORY   (United States)

Author keywords

Cd toxicity; Cd transport; Metal binding site; Zinc; Zn transporter

Indexed keywords

CADMIUM; HISTIDINE; ZINC;

ARTICLE; BINDING SITE; CHEMICAL STRUCTURE; CYTOPLASM; PHYLOGENY; PRIORITY JOURNAL;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BINDING SITES; BIOLOGICAL TRANSPORT; CADMIUM; CATION TRANSPORT PROTEINS; CYTOPLASM; ESCHERICHIA COLI PROTEINS; HEK293 CELLS; HISTIDINE; HUMANS; IMMUNOBLOTTING; KINETICS; MEMBRANE TRANSPORT PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; TRANSFECTION; ZINC;

BACTERIA (MICROORGANISMS); MAMMALIA;

EID: 84860803646     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1200362109     Document Type: Article

References (41)

1. Vallee BL, Falchuk KH (1993) The biochemical basis of zinc physiology. Physiol Rev 73:79-118. (Pubitemid 23065434)
2. Usuda K, et al. (2011) Toxicological aspects of cadmium and occupational health activities to prevent workplace exposure in Japan: A narrative review. Toxicol Ind Health 27:225-233.
3. Jarup L, Alfven T (2004) Low level cadmium exposure, renal and bone effects - the OSCAR study. Biometals 17:505-509. (Pubitemid 41214257)
4. Staessen JA, et al. (1999) Environmental exposure to cadmium, forearm bone density, and risk of fractures: prospective population study. Public Health and Environmental Exposure to Cadmium (PheeCad) Study Group. Lancet 353:1140-1144. (Pubitemid 29155207)
5. Dalton TP, et al. (2005) Identification of mouse SLC39A8 as the transporter responsible for cadmium-induced toxicity in the testis. Proc Natl Acad Sci USA 102:3401-3406. (Pubitemid 40328057)
6. Girijashanker K, et al. (2008) Slc39a14 gene encodes ZIP14, a metal/bicarbonate symporter: similarities to the ZIP8 transporter. Mol Pharmacol 73:1413-1423. (Pubitemid 351574831)
7. He L, et al. (2006) ZIP8, member of the solute-carrier-39 (SLC39) metal-transporter family: characterization of transporter properties. Mol Pharmacol 70:171-180.
8. Rising L, Vitarella D, Kimelberg HK, Aschner M (1995) Cadmium chloride (CdCl2)- induced metallothionein (MT) expression in neonatal rat primary astrocyte cultures. Brain Res 678:91-98.
9. Hong SH, Maret W, Brouwer M, Hoexum-Brouwer T, Cashon RE (2003) A putative glutathione-binding site in CdZn-metallothionein identified by equilibrium binding and molecular-modelling studies. Proc Natl Acad Sci USA 100:2255-2260.
10. Vitarella D, Conklin DR, Kimelberg HK, Aschner M (1996) Metallothionein induction protects swollen rat primary astrocyte cultures from methylmercury-induced inhibition of regulatory volume decrease. Brain Res 738:213-221. (Pubitemid 26378914)
11. Moreno I, et al. (2008) AtHMA1 is a thapsigargin-sensitive Ca2+/heavy metal pump. J Biol Chem 283:9633-9641.
12. Lewinson O, Lee AT, Rees DC (2009) A P-type ATPase importer that discriminates between essential and toxic transition metals. Proc Natl Acad Sci USA 106:4677-4682.
13. Ueno D, et al. (2010) Gene limiting cadmium accumulation in rice. Proc Natl Acad Sci USA 107:16500-16505.
14. Lutsenko S, Petris MJ (2003) Function and regulation of the mammalian copper-transporting ATPases: insights from biochemical and cell biological approaches. J Membr Biol 191:1-12. (Pubitemid 37011461)
15. Elinder CG, Lind B, Kjellstrom T, Linnman L, Friberg L (1976) Cadmium in kidney cortex, liver, and pancreas from Swedish autopsies. Estimation of biological half time in kidney cortex, considering calorie intake and smoking habits. Arch Environ Health 31:292-302. (Pubitemid 8005014)
16. Krebs NF (2000) Overview of zinc absorption and excretion in the human gastrointestinal tract. J Nutr 130:1374S-1377S.
17. Eide DJ (2006) Zinc transporters and the cellular trafficking of zinc. Biochim Biophys Acta 1763:711-722.
18. 2+ transporter. J Biol Chem 284:17677-17686.
19. Kambe T, et al. (2002) Cloning and characterization of a novel mammalian zinc transporter, zinc transporter 5, abundantly expressed in pancreatic beta cells. J Biol Chem 277:19049-19055. (Pubitemid 34952469)
20. Hinkle PM, Shanshala ED, II, Nelson EJ (1992) Measurement of intracellular cadmium with fluorescent dyes. Further evidence for the role of calcium channels in cadmium uptake. J Biol Chem 267:25553-25559.
21. 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 123:7831-7841. (Pubitemid 32899347)
22. Chimienti F, Devergnas S, Favier A, Seve M (2004) Identification and cloning of a beta-cell- specific zinc transporter, ZnT-8, localized into insulin secretory granules. Diabetes 53:2330-2337. (Pubitemid 39145586)
23. Chimienti F, et al. (2006) In vivo expression and functional characterization of the zinc transporter ZnT8 in glucose-induced insulin secretion. J Cell Sci 119:4199-4206. (Pubitemid 44774026)
24. Wei Y, Fu D (2005) Selective metal binding to a membrane-embedded aspartate in the Escherichia coli metal transporter YiiP (FieF). J Biol Chem 280:33716-33724. (Pubitemid 41443089)
25. Lu M, Fu D (2007) Structure of the zinc transporter YiiP. Science 317:1746-1748. (Pubitemid 47461838)
26. Chao Y, Fu D (2004) Kinetic study of the antiport mechanism of an Escherichia coli zinc transporter, ZitB. J Biol Chem 279:12043-12050. (Pubitemid 38445766)
27. Lu M, Chai J, Fu D (2009) Structural basis for autoregulation of the zinc transporter YiiP. Nat Struct Mol Biol 16:1063-1067.
28. Chao Y, Fu D (2004) Thermodynamic studies of the mechanism of metal binding to the Escherichia coli zinc transporter YiiP. J Biol Chem 279:17173-17180. (Pubitemid 38560474)
29. Wei Y, Fu D (2006) Binding and transport of metal ions at the dimer interface of the Escherichia coli metal transporter YiiP. J Biol Chem 281:23492-23502 Epub 22006 Jun 23421.
30. Forrest LR, Kramer R, Ziegler C (2011) The structural basis of secondary active transport mechanisms. Biochim Biophys Acta 1807:167-188.
31. Outten C, Halloran T (2001) Femtomolar sensitivity of metalloregulatory proteins controlling zinc homeostasis. Science 292:2488-2492. (Pubitemid 32605687)
32. Northrop DB (1998) On the meaning of Km and V/K in enzyme kinetics. J Chem Educ 75:1153-1157.
33. Palmiter RD, Cole TB, Findley SD (1996) ZnT-2, a mammalian protein that confers resistance to zinc by facilitating vesicular sequestration. EMBO J 15:1784-1791. (Pubitemid 26119214)
34. Doyle DA, et al. (1998) The structure of the potassium channel: molecular basis of K+ conduction and selectivity. Science 280:69-77. (Pubitemid 28169082)
35. Montanini B, Blaudez D, Jeandroz S, Sanders D, Chalot M (2007) Phylogenetic and functional analysis of the Cation Diffusion Facilitator (CDF) family: improved signature and prediction of substrate specificity. BMC Genomics 8:107-122.
36. Pang YP, Xu K, Yazal JE, Prendergas FG (2000) Successful molecular dynamics simulation of the zinc-bound farnesyltransferase using the cationic dummy atom approach. Protein Sci 9:1857-1865.
37. Podar D, et al. (2012) Metal selectivity determinants in a family of transition metal transporters. J Biol Chem 287:3185-3196.
38. Leszczyszyn OI, White CR, Blindauer CA (2010) The isolated Cys2His2 site in EC metallothionein mediates metal-specific protein folding. Mol Biosyst 6:1592-1603.
39. Sugita Y, Miyashita N, Ikeguchi M, Kidera A, Toyoshima C (2005) Protonation of the acidic residues in the transmembrane cation-binding sites of the ca(2+) pump. J Am Chem Soc 127:6150-6151. (Pubitemid 40627723)
40. Shils ME, Shike M, Ross AC, Caballero B, Cousins RJ, eds. (2005) Modern Nutrition in Health and Disease (Williams and Wilkins, Baltimore, MD), 10th Ed.
41. 2+ and regulates ion transport. Proc Natl Acad Sci USA 98:11749-11754.