2.A.5 The Zinc (Zn2+)-Iron (Fe2+) Permease (ZIP) Family

Most members of the ZIP family consist of 220-650 amino acyl residues with 8 TMSs. However, LIV1 of man has been reported to have only 6 TMSs, although it exhibits 8 hydrophobic peaks, and the IAA-alanine resistance protein 1 (Iar1 of A. thaliana) also exhibits 8 TMSs (Lasswell et al., 2000). They are derived from animals, plants, yeast, bacteria and archaea. They comprise a diverse family, with several paralogues in any one organism (e.g., 14 in mammals such as humans, at least 5 in Caenorhabditis elegans and Arabidopsis thaliana, 9 in maize and two in Saccharomyces cervisiae). Zinc homeostasis in plants has been reviewed (Ricachenevsky et al. 2015).  ZIP proteins form homo- or heterodimers with 8 transmembrane domains and extra-/intracellular domains of various lengths. Several ZIP members show specific extracellular domains composed of two subdomains, a helix-rich domain and proline-alanine-leucine (PAL) motif-containing domain (Bin et al. 2018).  ZIP genes in peanuts play crucial roles in the uptake and transport of Fe, Zn and Mn (Zhang et al. 2022). The structural bases for zinc transport through ZIP and ZnT porters, including the molecular mechanisms of zinc binding and transport, have been reviewed (Yin et al. 2022). Genome-wide functional studies of the ZIP family proteins in wild emmer wheat have been summarized (Gong et al. 2022). These proteins have the ZIP fold (Ferrada and Superti-Furga 2022). Zip family proteins have been reviewed (Ma and Gong 2023). The oligomeric state of ZIP transporters in mammalian cells have been estimated with fluorescence correlation spectroscopy (Liu et al. 2023).

The various mammalian paralogues fall into four subfamilies and are found in a variety of cell types, cell locations and tissues, and some are responsive to hormones and cytokines (Dempski 2012). Some mammalian Zip genes apparently do not  play critical roles in zinc homeostasis when zinc is replete, but they play important, noncompensatory roles when this metal is deficient (Kambe et al. 2008).  Zip6 (LIV1) is estrogen responsive in breast cancer cells and is related to metastasis in lymph nodes. Zip8 (Big M103) is TNFα and endotoxin induced in monocytes. The two S. cerevisiae proteins, Zrt1 and Zrt2, both probably transport Zn2+ with high specificity, but Zrt1 transports Zn2+ with ten-fold higher affinity than Zrt2. In cacao (Theobroma cacao L.) there are 11 ZIP homologs, and their physicochemical properties, evolution, duplication, gene structure, promoter region and TcZIP family three-dimensional protein structures are described in the plasma membrane and chloroplast (Pacheco et al. 2023).  Zinc transporters serve as prognostic predictors, and their expression correlates with immune cell infiltration in specific typoes of cancer (Liu et al. 2024).  SLC39 family genes influence cancer progression, immune infiltration, and drug sensitivity in multiple cancers (Qu et al. 2021).

Some members of the ZIP family have been shown to transport Zn2+ while others transport Fe2+, and a few have been shown to transport a range of metal ions. One human protein member of the ZIP family is designated ''growth arrest inducible gene product,'' but its presumed transport activity has not been identified. A second human protein, Zip4, is a Zn2+ uptake permease and a disease protein (Cousins et al., 2006). Histidine-rich repeats are found in extracellular N- and C-termini as well as a long intracellular loop, and Zip14 has an extra extracellular his-rich loop. One family of mammalian Zip proteins (the LZT family) has a metaprotease motif (HEXPHEXGD) that may allow them to function as matrix metaloproteases. Zip10 has C2H2 zinc finger and cytochrome c motifs in its first TMS (Cousins et al., 2006). Flavanones such as 5,4'-dihydroxyflavone (DHF) primarily affects the  transcription of iron and zinc ion transport genes (Yu et al. 2023).

The energy source for transport has not been characterized, but these systems probably function as secondary carriers. They do not require ATP (Cousins et al., 2006). In one study, uptake of Zn2+ via the hZip2 permease was energy independent, independent of Na+ and K+ gradients, but stimulated by HCO3- (Gaither and Eide, 2000). The authors propose a Zn2+:HCO3- symport mechanism. hZip1 is the major Zn2+ uptake system in many human tissues (Gaither and Eide, 2001). The N-terminal regions are novel substrate selectors in the ZIP family of transporters (Nishida et al., 2011). An inward-open metal-free BbZIP structure differs substantially in the relative positions of the two separate domains of ZIPs. With accompanying coevolutional analyses, mutagenesis, and uptake assays, the data point to an elevator-type transport mechanism, likely shared within the ZIP family, unifying earlier functional data. Moreover, the structure reveals a previously unknown ninth transmembrane segment that is important for activity in vivo (Wiuf et al. 2022).

Mice deficient in Zn transporter Slc39a13/Zip13 show changes in bone, teeth, and connective tissues, reminiscent of the clinical spectrum of human Ehlers-Danlos syndrome (EDS), of some features of osteogenesis imperfecta and Zn deficient disorders. The Zip13 knockout (Zip13-KO) mice show defects in the function of osteoblasts, chondrocytes, odontoblasts and fibroblasts. Zip13 protein is localized to the Golgi in the corresponding cells. Impairment in BMP and TGF-beta signaling were observed in Zip13-KO cells (Fukada et al., 2008).  ZIP5, ZIP6, ZIP7, and ZIP10 in rat liver are regulated by iron. They may play a role in hepatic iron/metal homeostasis during iron deficiency and overload (Nam and Knutson, 2012).  In maize, IRT1 is induced by zinc and iron deficiency, ZIP4 is induced during early embryogeneis, ZIP5 is induced during middle embryogeneis, and IRT1 and ZIP6 are induced during late embryogenesis (Li et al. 2013). 

12 members of the Zn/Fe-regulated transporters (ZRT/IRT) (ZIP Family) have been identified and isolated from Poncirus trifoliata, and they were named PtZIPs according to the sequence and functional similarity to Arabidopsis thaliana ZIPs (Fu et al. 2017). The 12 PtZIPs are of 334-419 aas, harboring 6-9 putative TMSs. All contain the conserved ZIP signature sequences in TMS4, and nine of them showed a variable region rich in histidine residues between TMS3 and TMS4.  PtZIPs fall into four phylogenetic groups as for ZIPs of A. thaliana. Expression analyses showed that PtZIP genes are differently induced in roots and leaves under conditions of Zn2+, Fe2+ and Mn2+ deficiency. PtIRT1, PtZIP1, PtZIP2, PtZIP3, and PtZIP12  complement a zrt1 zrt2 mutant, which was deficient in Zn2+ uptake; PtIRT1 and PtZIP7 complement a fet3 fet4 mutant, deficient in Fe2+ uptake, and PtIRT1 complements a smf1 mutant, deficient in Mn2+ uptake, suggesting their respective functions in Zn2+, Fe2+, and Mn2+ transport (Fu et al. 2017).

There are 10 ZnT (CDF) (TC#2.A.4) and 15 Zip transporters in humans. They appear to play opposite roles in cellular zinc homeostasis. CDF transporters reduce intracellular zinc availability by promoting zinc efflux from cells or into intracellular vesicles, while Zip transporters increase intracellular zinc availability by promoting extracellular zinc uptake and vesicular zinc release into the cytoplasm. Both the ZnT and Zip transporter families exhibit unique tissue-specific expression, differential responsiveness to dietary zinc deficiency and excess, and differential responsiveness to physiologic stimuli via hormones and cytokines (Liuzzi and Cousins 2004).

The apo state structure in an inward-facing conformation from Bordetella bronchiseptica revealed a disassembled transport site, altered inter-helical interactions, and a rigid body movement of a 4 TMS bundle relative to the other TMSs (Zhang et al. 2023). The computationally generated and biochemically validated outward-facing conformation model revealed a slide of the 4-TMS bundle, which carries the transport site(s), by approximately 8 Å toward the extracellular side against the static TMSs which mediate dimerization. Thus, BbZIP is an elevator-type transporter. Pang et al. 2023 reported a cryo-EM structure of a ZIP-family transporter from Bordetella bronchiseptica at 3.05 Å resolution in an inward-facing, inhibited conformation. The transporter forms a homodimer, each protomer containing nine transmembrane helices and three metal ions. Two metal ions form a binuclear pore structure, and the third ion is located at an egress site facing the cytoplasm. The egress site is covered by a loop, and two histidine residues on the loop interact with the egress-site ion and regulate its release. Cell-based Zn2+ uptake and cell growth viability assays revealed negative regulation of Zn2+ uptake through sensing intracellular Zn2+ status using a built-in sensor. These analyses provided mechanistic insight into the autoregulation of zinc uptake across membranes (Pang et al. 2023).

The generalized transport reaction for members of the ZIP family is:

Me2+ (out) (pmf) → Me2+ (in)


 

References:

Antala S., Ovchinnikov S., Kamisetty H., Baker D. and Dempski RE. (2015). Computation and Functional Studies Provide a Model for the Structure of the Zinc Transporter hZIP4. J Biol Chem. 290(29):17796-805.

Bafaro EM., Antala S., Nguyen TV., Dzul SP., Doyon B., Stemmler TL. and Dempski RE. (2015). The large intracellular loop of hZIP4 is an intrinsically disordered zinc binding domain. Metallomics. 7(9):1319-30.

Bellotti, D., A. Miller, M. Rowińska-Żyrek, and M. Remelli. (2022). Zn and Cu Binding to the Extramembrane Loop of Zrt2, a Zinc Transporter of. Biomolecules 12:.

Berg AH., Rice CD., Rahman MS., Dong J. and Thomas P. (2014). Identification and characterization of membrane androgen receptors in the ZIP9 zinc transporter subfamily: I. Discovery in female atlantic croaker and evidence ZIP9 mediates testosterone-induced apoptosis of ovarian follicle cells. Endocrinology. 155(11):4237-49.

Bin, B.H., J. Seo, and S.T. Kim. (2018). Function, Structure, and Transport Aspects of ZIP and ZnT Zinc Transporters in Immune Cells. J Immunol Res 2018: 9365747.

Bin, B.H., T. Fukada, T. Hosaka, S. Yamasaki, W. Ohashi, S. Hojyo, T. Miyai, K. Nishida, S. Yokoyama, and T. Hirano. (2011). Biochemical characterization of human ZIP13 protein: a homo-dimerized zinc transporter involved in the spondylocheiro dysplastic Ehlers-Danlos syndrome. J. Biol. Chem. 286: 40255-40265.

Boch, A., A. Trampczynska, C. Simm, N. Taudte, U. Krämer, and S. Clemens. (2008). Loss of Zhf and the tightly regulated zinc-uptake system SpZrt1 in Schizosaccharomyces pombe reveals the delicacy of cellular zinc balance. FEMS Yeast Res 8: 883-896.

Breitwieser, W., C. Price, and T. Schuster. (1993). Identification of a gene encoding a novel zinc finger protein in Saccharomyces cerevisiae. Yeast 9: 551-556.

Chanket, W., M. Pipatthana, A. Sangphukieo, P. Harnvoravongchai, S. Chankhamhaengdecha, T. Janvilisri, and M. Phanchana. (2024). The complete catalog of antimicrobial resistance secondary active transporters in : evolution and drug resistance perspective. Comput Struct Biotechnol J 23: 2358-2374.

Choi, E.K., L. Aring, Y. Peng, A.B. Correia, A.P. Lieberman, S. Iwase, and Y.A. Seo. (2024). Neuron.al SLC39A8 deficiency impairs cerebellar development by altering manganese homeostasis. JCI Insight 9:.

Citiulo, F., I.D. Jacobsen, P. Miramón, L. Schild, S. Brunke, P. Zipfel, M. Brock, B. Hube, and D. Wilson. (2012). Candida albicans scavenges host zinc via Pra1 during endothelial invasion. PLoS Pathog 8: e1002777.

Cousins, R.J., J.P. Liuzzi, and L.A. Lichten. (2006). Mammalian zinc transport, trafficking, and signals. J. Biol. Chem. 281: 24085-24089.

Dechen, K., C.D. Richards, J.C. Lye, J.E. Hwang, and R. Burke. (2015). Compartmentalized zinc deficiency and toxicities caused by ZnT and Zip gene over expression result in specific phenotypes in Drosophila. Int J Biochem. Cell Biol. 60: 23-33.

Dempski, R.E. (2012). The Cation Selectivity of the ZIP Transporters. Curr Top Membr 69: 221-245.

Diallinas, G. (2017). Transceptors as a functional link of transporters and receptors. Microb Cell 4: 69-73.

Duan, M. and T. Zhang. (2023). Expression, purification, and crystallization of the extracellular domain of a mammalian ZIP4. Methods Enzymol 687: 49-65.

Dufner-Beattie J., S.J. Langmade, F. Wang, D. Eide, G.K. Andrews. (2003). Structure, function, and regulation of a subfamily of mouse zinc transporter genes. J. Biol. Chem. 278: 50142-50150.

Dufner-Beattie, J., F. Wang, Y.M. Kuo, J. Gitschier, D. Eide, and G.K. Andrews. (2003). The Acrodermatitis enteropathica gene ZIP4 encodes a tissue-specific, zinc-regulated zinc transporter in mice. J. Biol Chem. 278: 33474-33481.

Dufner-Beattie, J., Z.L. Huang, J. Geiser, W. Xu, and G.K. Andrews. (2005). Generation and characterization of mice lacking the zinc uptake transporter ZIP3. Mol. Cell Biol. 25: 5607-5615.

Ehsani, S., A. Salehzadeh, H. Huo, W. Reginold, C.L. Pocanschi, H. Ren, H. Wang, K. So, C. Sato, M. Mehrabian, R. Strome, W.S. Trimble, L.N. Hazrati, E. Rogaeva, D. Westaway, G.A. Carlson, and G. Schmitt-Ulms. (2012). LIV-1 ZIP ectodomain shedding in prion-infected mice resembles cellular response to transition metal starvation. J. Mol. Biol. 422: 556-574.

Eide, D. and M.L. Guerinot. (1997). Metal ion uptake in eukaryotes. ASM News 63: 199-205.

Eide, D., M. Broderius, J. Fett, and M.L. Guerinot. (1996). A novel iron-regulated metal transporter from plants identified by functional expression in yeast. Proc. Natl. Acad. Sci. USA 93: 5624-5628.

Eng, B.H., M.L. Guerinot, D. Eide, and M.H. Saier, Jr. (1998). Sequence analyses and phylogenetic characterization of the ZIP family of metal ion transport proteins. J. Membr. Biol. 166: 1-7.

Fasani, E., G. DalCorso, G. Zorzi, C. Agrimonti, R. Fragni, G. Visioli, and A. Furini. (2021). Overexpression of ZNT1 and NRAMP4 from the Ni Hyperaccumulator Population Monte Prinzera in Perturbs Fe, Mn, and Ni Accumulation. Int J Mol Sci 22:.

Ferdigg, A., A.K. Hopp, G. Wolf, and G. Superti-Furga. (2025). Membrane transporters modulating the toxicity of arsenic, cadmium, and mercury in human cells. Life Sci Alliance 8:.

Ferrada, E. and G. Superti-Furga. (2022). A structure and evolutionary-based classification of solute carriers. iScience 25: 105096.

Fu, X.Z., X. Zhou, F. Xing, L.L. Ling, C.P. Chun, L. Cao, M.G.M. Aarts, and L.Z. Peng. (2017). Genome-Wide Identification, Cloning and Functional Analysis of the Zinc/Iron-Regulated Transporter-Like Protein (ZIP) Gene Family in Trifoliate Orange (Poncirus trifoliata L. Raf.). Front Plant Sci 8: 588.

Fujishiro, H., S. Miyamoto, D. Sumi, T. Kambe, and S. Himeno. (2022). Effects of individual amino acid mutations of zinc transporter ZIP8 on manganese- and cadmium-transporting activity. Biochem. Biophys. Res. Commun. 616: 26-32.

Fukada, T., N. Civic, T. Furuichi, S. Shimoda, K. Mishima, H. Higashiyama, Y. Idaira, Y. Asada, H. Kitamura, S. Yamasaki, S. Hojyo, M. Nakayama, O. Ohara, H. Koseki, H.G. Dos Santos, L. Bonafe, R. Ha-Vinh, A. Zankl, S. Unger, M.E. Kraenzlin, J.S. Beckmann, I. Saito, C. Rivolta, S. Ikegawa, A. Superti-Furga, and T. Hirano. (2008). The zinc transporter SLC39A13/ZIP13 is required for connective tissue development; its involvement in BMP/TGF-beta signaling pathways. PLoS One 3: e3642.

Gaither, L.A. and D.J. Eide. (2000). Functional expression of the human hZIP2 zinc transporter. J. Biol. Chem. 275: 5560-5564.

Gaither, L.A. and D.J. Eide. (2001). The human ZIP1 transporter mediates zinc uptake in human K562 erythroleukemia cells. J. Biol. Chem. 276: 22258-22264.

Garstka, K., A. Hecel, H. Kozłowski, and M. Rowińska-Żyrek. (2022). Specific Zn(II)-binding site in the C-terminus of Aspf2, a zincophore from Aspergillus fumigatus. Metallomics 14:.

Giacconi, R., L. Costarelli, M. Malavolta, M. Cardelli, R. Galeazzi, F. Piacenza, N. Gasparini, A. Basso, E. Mariani, T. Fulop, L. Rink, G. Dedoussis, G. Herbein, J. Jajte, M. Provinciali, F. Busco, and E. Mocchegiani. (2015). Effect of ZIP2 Gln/Arg/Leu (rs2234632) polymorphism on zinc homeostasis and inflammatory response following zinc supplementation. Biofactors. [Epub: Ahead of Print]

Gomes, D.S., C.J. Riger, M.L. Pinto, A.D. Panek, and E.C. Eleutherio. (2005). Evaluation of the role of Ace1 and Yap1 in cadmium absorption using the eukaryotic cell model Saccharomyces cerevisiae. Environ Toxicol Pharmacol 20: 383-389.

Gong, F., T. Qi, Y. Hu, Y. Jin, J. Liu, W. Wang, J. He, B. Tu, T. Zhang, B. Jiang, Y. Wang, L. Zhang, Y. Zheng, D. Liu, L. Huang, and B. Wu. (2022). Genome-Wide Investigation and Functional Verification of the ZIP Family Transporters in Wild Emmer Wheat. Int J Mol Sci 23:.

Gong, M., C. Peng, C. Yang, Z. Wang, H. Qian, X. Hu, P. Zhou, C. Shan, and Q. Ding. (2024). Genome-wide CRISPR/Cas9 screen identifies SLC39A9 and PIK3C3 as crucial entry factors for Ebola virus infection. PLoS Pathog 20: e1012444.

Grass, G., S. Franke, N. Taudte, D.H. Nies, L.M. Kucharski, M.E. Maguire, and C. Rensing. (2005). The metal permease ZupT from Escherichia coli is a transporter with a broad substrate spectrum. J. Bacteriol. 187: 1604-1611.

Grotz, N., T. Fox, E. Connolly, W. Park, M.L. Guerinot, and D. Eide. (1998). Identification of a family of zinc transporter genes from Arabidopsis that respond to zinc deficiency. Proc. Natl. Acad. Sci. USA 95: 7220-7224.

Grover, A., and Sharma R. (2006). Identification and Characterization of a Major Zn(II) Resistance Determinant of Mycobacterium smegmatis. J. Bact. 188: 7026-7032.

Gupta, S., C. Merriman, C.J. Petzold, C. Ralston, and D. Fu. (2019). Water molecules mediate zinc mobility in the bacterial zinc diffusion channel ZIPB. J. Biol. Chem. [Epub: Ahead of Print]

Halimaa, P., Y.F. Lin, V.H. Ahonen, D. Blande, S. Clemens, A. Gyenesei, E. Häikiö, S.O. Kärenlampi, A. Laiho, M.G. Aarts, J.P. Pursiheimo, H. Schat, H. Schmidt, M.H. Tuomainen, and A.I. Tervahauta. (2014). Gene Expression Differences between Noccaea caerulescens Ecotypes Help to Identify Candidate Genes for Metal Phytoremediation. Environ Sci Technol 48: 3344-3353.

Han, T.L., T.W. Tang, P.H. Zhang, M. Liu, J. Zhao, J.S. Peng, and S. Meng. (2022). Cloning and Functional Characterization of. Genes (Basel) 13:.

Herzberg, M., L. Bauer, and D.H. Nies. (2014). Deletion of the zupT gene for a zinc importer influences zinc pools in Cupriavidus metallidurans CH34. Metallomics 6: 421-436.

Huang, L., C.P. Kirschke, Y. Zhang, and Y.Y. Yu. (2005). The ZIP7 gene (Slc39a7) encodes a zinc transporter involved in zinc homeostasis of the Golgi apparatus. J. Biol. Chem. 280: 15456-15463.

Hudek L., Pearson LA., Michalczyk A., Neilan BA. and Ackland ML. (2013). Functional characterization of the twin ZIP/SLC39 metal transporters, NpunF3111 and NpunF2202 in Nostoc punctiforme. Appl Microbiol Biotechnol. 97(19):8649-62.

Huynh, C. and N.W. Andrews. (2008). Iron acquisition within host cells and the pathogenicity of Leishmania. Cell Microbiol 10: 293-300.

Huynh, C., D.L. Sacks, and N.W. Andrews. (2006). A Leishmania amazonensis ZIP family iron transporter is essential for parasite replication within macrophage phagolysosomes. J Exp Med 203: 2363-2375.

Ishida, H., R. Yo, Z. Zhang, T. Shimizu, and U. Ohto. (2024). Cryo-EM structures of the zinc transporters ZnT3 and ZnT4 provide insights into their transport mechanisms. FEBS Lett. [Epub: Ahead of Print]

Ivanov, R., T. Brumbarova, A. Blum, A.M. Jantke, C. Fink-Straube, and P. Bauer. (2014). SORTING NEXIN1 is required for modulating the trafficking and stability of the Arabidopsis IRON-REGULATED TRANSPORTER1. Plant Cell 26: 1294-1307.

Jacques, I., N.W. Andrews, and C. Huynh. (2010). Functional characterization of LIT1, the Leishmania amazonensis ferrous iron transporter. Mol Biochem Parasitol 170: 28-36.

Jenkitkasemwong, S., A. Akinyode, E. Paulus, R. Weiskirchen, S. Hojyo, T. Fukada, G. Giraldo, J. Schrier, A. Garcia, C. Janus, B. Giasson, and M.D. Knutson. (2018). SLC39A14 deficiency alters manganese homeostasis and excretion resulting in brain manganese accumulation and motor deficits in mice. Proc. Natl. Acad. Sci. USA. [Epub: Ahead of Print]

Jenkitkasemwong, S., C.Y. Wang, B. Mackenzie, and M.D. Knutson. (2012). Physiologic implications of metal-ion transport by ZIP14 and ZIP8. Biometals 25: 643-655.

Juneja, M., U. Shamim, A. Joshi, A. Mathur, B. Uppili, S. Sairam, S. Ambawat, R. Dixit, and M. Faruq. (2018). A novel mutation in SLC39A14 causing hypermanganesemia associated with infantile onset dystonia. J Gene Med 20: e3012.

Kagara, N., N. Tanaka, S. Noguchi, and T. Hirano. (2007). Zinc and its transporter ZIP10 are involved in invasive behavior of breast cancer cells. Cancer Sci. 98: 692-697.

Kambe, T., J. Geiser, B. Lahner, D.E. Salt, and G.K. Andrews. (2008). Slc39a1 to 3 (subfamily II) Zip genes in mice have unique cell-specific functions during adaptation to zinc deficiency. Am. J. Physiol. Regul Integr Comp Physiol 294: R1474-1481.

Karlinsey, J.E., M.E. Maguire, L.A. Becker, M.L. Crouch, and F.C. Fang. (2010). The phage shock protein PspA facilitates divalent metal transport and is required for virulence of Salmonella enterica sv. Typhimurium. Mol. Microbiol. 78: 669-685.

Kiener, S., R. Cikota, M. Welle, V. Jagannathan, S. Åhman, and T. Leeb. (2021). A Missense Variant in in a Litter of Turkish Van Cats with Acrodermatitis Enteropathica. Genes (Basel) 12:.

Korshunova, Y.O., D. Eide, W.G. Clark, M.L. Guerinot, and H.B. Pakrasi. (1999). The IRT1 protein from Arabidopsis thaliana is a metal transporter with a broad substrate range. Plant Mol. Biol. 40: 37-44.

Kuliyev, E., C. Zhang, D. Sui, and J. Hu. (2021). Zinc transporter mutations linked to acrodermatitis enteropathica disrupt function and cause mistrafficking. J. Biol. Chem. 296: 100269. [Epub: Ahead of Print]

Kumanovics, A., K.E. Poruk, K.A. Osborn, D.M. Ward, and J. Kaplan. (2006). YKE4 (YIL023C) encodes a bidirectional zinc transporter in the endoplasmic reticulum of Saccharomyces cerevisiae. J. Biol. Chem. 281: 22566-22574.

Lasswell, J., L.E. Rogg, D.C. Nelson, C. Rongey, and B. Bartel. (2000). Cloning and characterization of IAR1, a gene required for auxin conjugate sensitivity in Arabidopsis. Plant Cell 12: 2395-2408.

Leonhardt, T., J. Sácký, and P. Kotrba. (2018). Functional analysis RaZIP1 transporter of the ZIP family from the ectomycorrhizal Zn-accumulating Russula atropurpurea. Biometals 31: 255-266.

Li S., Zhou X., Huang Y., Zhu L., Zhang S., Zhao Y., Guo J., Chen J. and Chen R. (2013). Identification and characterization of the zinc-regulated transporters, iron-regulated transporter-like protein (ZIP) gene family in maize. BMC Plant Biol. 13:114.

Liang, Z.L., H.W. Tan, J.Y. Wu, X.L. Chen, X.Y. Wang, Y.M. Xu, and A.T.Y. Lau. (2021). The Impact of ZIP8 Disease-Associated Variants G38R, C113S, G204C, and S335T on Selenium and Cadmium Accumulations: The First Characterization. Int J Mol Sci 22:.

Lin, S.J. and V.C. Culotta. (1996). Suppression of oxidative damage by Saccharomyces cerevisiae ATX2, which encodes a manganese-trafficking protein that localizes to Golgi-like vesicles. Mol. Cell. Biol. 16: 6303-6312.

Lin, W., J. Chai, J. Love, and D. Fu. (2010). Selective electrodiffusion of zinc ions in a Zrt-, Irt-like protein, ZIPB. J. Biol. Chem. 285: 39013-39020.

Liu, Y., E.M. Bafaro, A.E. Cowan, and R.E. Dempski. (2022). The transmembrane domains mediate oligomerization of the human ZIP4 transporter in vivo. Sci Rep 12: 21083.

Liu, Y., E.M. Bafaro, and R.E. Dempski. (2022). Heterologous Expression of Full-Length and Truncated Human ZIP4 Zinc Transporter in. Biomolecules 12:.

Liu, Y., E.M. Bafaro, and R.E. Dempski. (2023). Single-molecule quantification of the oligomeric state of ZIP transporters in mammalian cells with fluorescence correlation spectroscopy. Methods Enzymol 687: 103-137.

Liu, Y., L. Wei, Z. Zhu, S. Ren, H. Jiang, Y. Huang, X. Sun, X. Sui, L. Jin, and X. Sun. (2024). Zinc Transporters Serve as Prognostic Predictors and their Expression Correlates with Immune Cell Infiltration in Specific Cancer: A Pan-cancer Analysis. J Cancer 15: 939-954.

Liu, Z., H. Li, M. Soleimani, K. Girijashanker, J.M. Reed, L. He, T.P. Dalton, and D.W. Nebert. (2008). Cd2+ versus Zn2+ uptake by the ZIP8 HCO3--dependent symporter: kinetics, electrogenicity and trafficking. Biochem. Biophys. Res. Commun. 365: 814-820.

López-Millán, A.F., D.R. Ellis, and M.A. Grusak. (2004). Identification and characterization of several new members of the ZIP family of metal ion transporters in Medicago truncatula. Plant Mol. Biol. 54: 583-596.

Lye, J.C., C.D. Richards, K. Dechen, C.G. Warr, and R. Burke. (2013). In vivo zinc toxicity phenotypes provide a sensitized background that suggests zinc transport activities for most of the Drosophila Zip and ZnT genes. J Biol Inorg Chem 18: 323-332.

Ma, C. and C. Gong. (2023). Considerations in production of the prokaryotic ZIP family transporters for structural and functional studies. Methods Enzymol 687: 1-30.

Nam H., Wang CY., Zhang L., Zhang W., Hojyo S., Fukada T. and Knutson MD. (2013). ZIP14 and DMT1 in the liver, pancreas, and heart are differentially regulated by iron deficiency and overload: implications for tissue iron uptake in iron-related disorders. Haematologica. 98(7):1049-57.

Nam, H. and M.D. Knutson. (2012). Effect of dietary iron deficiency and overload on the expression of ZIP metal-ion transporters in rat liver. Biometals 25: 115-124.

Nishida, S., Y. Morinaga, H. Obata, and T. Mizuno. (2011). Identification of the N-terminal region of TjZNT2, a Zrt/Irt-like protein family metal transporter, as a novel functional region involved in metal ion selectivity. FEBS J. 278: 851-858.

Pacheco, D.D.R., B.C.G. Santana, C.P. Pirovani, and A.F. de Almeida. (2023). Zinc/iron-regulated transporter-like protein gene family in L: Characteristics, evolution, function and 3D structure analysis. Front Plant Sci 14: 1098401.

Pang, C., J. Chai, P. Zhu, J. Shanklin, and Q. Liu. (2023). Structural mechanism of intracellular autoregulation of zinc uptake in ZIP transporters. Nat Commun 14: 3404.

Pinilla-Tenas, J.J., B.K. Sparkman, A. Shawki, A.C. Illing, C.J. Mitchell, N. Zhao, J.P. Liuzzi, R.J. Cousins, M.D. Knutson, and B. Mackenzie. (2011). Zip14 is a complex broad-scope metal-ion transporter whose functional properties support roles in the cellular uptake of zinc and nontransferrin-bound iron. Am. J. Physiol. Cell Physiol. 301: C862-871.

Plaza, S., K.L. Tearall, F.J. Zhao, P. Buchner, S.P. McGrath, and M.J. Hawkesford. (2007). Expression and functional analysis of metal transporter genes in two contrasting ecotypes of the hyperaccumulator Thlaspi caerulescens. J Exp Bot 58: 1717-1728.

Potocki S., Valensin D. and Kozlowski H. (2014). The specificity of interaction of Zn(2+), Ni(2+) and Cu(2+) ions with the histidine-rich domain of the TjZNT1 ZIP family transporter. Dalton Trans. 43(26):10215-23.

Powers, M., D. Minchella, M. Gonzalez-Acevedo, D. Escutia-Plaza, J. Wu, C. Heger, G. Milne, M. Aschner, and Z. Liu. (2023). Loss of hepatic manganese transporter ZIP8 disrupts serum transferrin glycosylation and the glutamate-glutamine cycle. J Trace Elem Med Biol 78: 127184. [Epub: Ahead of Print]

Qu, Y.Y., R.Y. Guo, M.L. Luo, and Q. Zhou. (2021). Pan-Cancer Analysis of the Solute Carrier Family 39 Genes in Relation to Oncogenic, Immune Infiltrating, and Therapeutic Targets. Front Genet 12: 757582.

Quintana, J., M. Bernal, M. Scholle, H. Holländer-Czytko, N.T. Nguyen, M. Piotrowski, D.G. Mendoza-Cózatl, M.J. Haydon, and U. Krämer. (2022). Root-to-shoot iron partitioning in Arabidopsis requires IRON-REGULATED TRANSPORTER1 (IRT1) protein but not its iron(II) transport function. Plant J. 109: 992-1013.

Radisky, D. and J. Kaplan. (1999). Regulation of transition metal transport across the yeast plasma membrane. J. Biol. Chem. 274: 4481-4484.

Ricachenevsky, F.K., P.K. Menguer, R.A. Sperotto, and J.P. Fett. (2015). Got to hide your Zn away: Molecular control of Zn accumulation and biotechnological applications. Plant Sci 236: 1-17.

Roberts, C.S., F. Ni, and B. Mitra. (2021). The Zinc and Iron Binuclear Transport Center of ZupT, a ZIP Transporter from. Biochemistry 60: 3738-3752.

Rodrigues, W.F.C., A.B.P. Lisboa, J.E. Lima, F.K. Ricachenevsky, and L.E. Del-Bem. (2023). Ferrous iron uptake via IRT1/ZIP evolved at least twice in green plants. New Phytol 237: 1951-1961.

Sampah, M.E.S., H. Moore, R. Ahmad, J. Duess, P. Lu, C. Lopez, S. Steinway, D. Scheese, Z. Raouf, K. Tsuboi, J. Ding, C. Caputo, M. McFarland, W.B. Fulton, S. Wang, M. Wang, T. Prindle, V. Gazit, D.C. Rubin, S. Alaish, C.P. Sodhi, and D.J. Hackam. (2024). Xenotransplanted human organoids identify transepithelial zinc transport as a key mediator of intestinal adaptation. Nat Commun 15: 8613.

Schaaf, G., A. Honsbein, A.R. Meda, S. Kirchner, D. Wipf, and N. von Wiren. (2006). AtIREG2 encodes a tonoplast transport protein involved in iron-dependent nickel detoxification in Arabidopsis thaliana roots. J. Biol. Chem. 281: 25532-25540.

Schmitt-Ulms, G., S. Ehsani, J.C. Watts, D. Westaway, and H. Wille. (2009). Evolutionary descent of prion genes from the ZIP family of metal ion transporters. PLoS One 4: e7208.

Schothorst, J., G.V. Zeebroeck, and J.M. Thevelein. (2017). Identification of Ftr1 and Zrt1 as iron and zinc micronutrient transceptors for activation of the PKA pathway in Saccharomyces cerevisiae. Microb Cell 4: 74-89.

Taudte N. and Grass G. (2010). Point mutations change specificity and kinetics of metal uptake by ZupT from Escherichia coli. Biometals. 23(4):643-56.

Taylor, K.M. and R.I. Nicholson. (2003). The LZT proteins: the LIV-1 subfamily of zinc transporters. Biochim. Biophys. Acta 1611: 16-30.

Ueno, M., K. Imadome, M. Iwakawa, K. Anzai, N. Ikota, and T. Imai. (2010). Vascular homeostasis regulators, Edn1 and Agpt2, are upregulated as a protective effect of heat-treated zinc yeast in irradiated murine bone marrow. J Radiat Res (Tokyo) 51: 519-525.

Wiuf, A., J.H. Steffen, E.R. Becares, C. Grønberg, D.R. Mahato, S.G.F. Rasmussen, M. Andersson, T. Croll, K. Gotfryd, and P. Gourdon. (2022). The two-domain elevator-type mechanism of zinc-transporting ZIP proteins. Sci Adv 8: eabn4331.

Xin, Y., H. Gao, J. Wang, Y. Qiang, M.U. Imam, Y. Li, J. Wang, R. Zhang, H. Zhang, Y. Yu, H. Wang, H. Luo, C. Shi, Y. Xu, S. Hojyo, T. Fukada, J. Min, and F. Wang. (2017). Manganese transporter Slc39a14 deficiency revealed its key role in maintaining manganese homeostasis in mice. Cell Discov 3: 17025.

Yamashita, S., C. Miyagi, T. Fukada, N. Kagara, Y.-S. Che, and T. Hirano. (2004). Zinc transporter LIVI controls epithelial-mesenchymal transition in zebrafish gastrula organizer. Nature 429: 298-302.

Yin, S., M. Duan, B. Fang, G. Zhao, X. Leng, and T. Zhang. (2022). Zinc homeostasis and regulation: Zinc transmembrane transport through transporters. Crit Rev Food Sci Nutr 1-11. [Epub: Ahead of Print]

Yu, R., Y. Chang, P. Pang, Y. Suo, and G. Gao. (2020). [In silico cloning, expression and bioinformatics analysis of StZnT11 in Solanum tuberosum]. Sheng Wu Gong Cheng Xue Bao 36: 362-371.

Yu, S., C. Xu, T. Tang, Y. Zhang, K. Effiong, J. Hu, Y. Bi, and X. Xiao. (2023). Down-regulation of iron/zinc ion transport and toxin synthesis in Microcystis aeruginosa exposed to 5,4''-dihydroxyflavone. J Hazard Mater 460: 132396.

Yu, Y., A. Wu, Z. Zhang, G. Yan, F. Zhang, L. Zhang, X. Shen, R. Hu, Y. Zhang, K. Zhang, and F. Wang. (2013). Characterization of the GufA subfamily member SLC39A11/Zip11 as a zinc transporter. J Nutr Biochem 24: 1697-1708.

Zhang, P., S. Tan, J.O. Berry, P. Li, N. Ren, S. Li, G. Yang, W.B. Wang, X.T. Qi, and L.P. Yin. (2014). An uncleaved signal peptide directs the Malus xiaojinensis iron transporter protein Mx IRT1 into the ER for the PM secretory pathway. Int J Mol Sci 15: 20413-20433.

Zhang, R., K. Witkowska, F. Ng, M.J. Caulfield, and S. Ye. (2015). LB03.08: HYPERTENSION RELATED VARIANT OF SOLUTE CARRIER FAMILY 39 MEMBER 8 GENE INFLUENCES CADMIUM UPTAKE AND CELL TOXICITY. J Hypertens 33Suppl1: e128.

Zhang, V., S. Jenkitkasemwong, Q. Liu, T. Ganz, E. Nemeth, M.D. Knutson, and A. Kim. (2023). A mouse model characterizes the roles of ZIP8 in systemic iron recycling and lung inflammation and infection. Blood Adv 7: 1336-1349.

Zhang, W., J. Song, S. Yue, K. Duan, and H. Yang. (2019). MhMAPK4 from Malus hupehensis Rehd. decreases cell death in tobacco roots by controlling Cd uptake. Ecotoxicol Environ Saf 168: 230-240.

Zhang, Y., D. Sui, and J. Hu. (2023). Expression, purification, crystallization of a ZIP metal transporter from Bordetella bronchiseptica (BbZIP). Methods Enzymol 687: 31-48.

Zhang, Y., Y. Jiang, K. Gao, D. Sui, P. Yu, M. Su, G.W. Wei, and J. Hu. (2023). Structural insights into the elevator-type transport mechanism of a bacterial ZIP metal transporter. Nat Commun 14: 385.

Zhang, Z., N. Chen, Z. Zhang, and G. Shi. (2022). Genome-Wide Identification and Expression Profile Reveal Potential Roles of Peanut Family Genes in Zinc/Iron-Deficiency Tolerance. Plants (Basel) 11:.

Zhao, H. and D. Eide. (1996). The ZRT2 gene encodes the low affinity zinc transporter in Saccharomyces cerevisiae. J. Biol. Chem. 271: 23203-23210.

Zhao, M. and B. Zhou. (2019). A distinctive sequence motif in the fourth transmembrane domain confers ZIP13 iron function in Drosophila melanogaster. Biochim. Biophys. Acta. Mol. Cell Res 1867: 118607. [Epub: Ahead of Print]

Zhao, N., J. Gao, C.A. Enns, and M.D. Knutson. (2010). ZRT/IRT-like protein 14 (ZIP14) promotes the cellular assimilation of iron from transferrin. J. Biol. Chem. 285: 32141-32150.

Zhao, Y., C.H. Tan, A. Krauchunas, A. Scharf, N. Dietrich, K. Warnhoff, Z. Yuan, M. Druzhinina, S.G. Gu, L. Miao, A. Singson, R.E. Ellis, and K. Kornfeld. (2018). The zinc transporter ZIPT-7.1 regulates sperm activation in nematodes. PLoS Biol 16: e2005069.

Łoboda, D. and M. Rowińska-Żyrek. (2017). Zinc binding sites in Pra1, a zincophore from Candida albicans. Dalton Trans. [Epub: Ahead of Print]

Examples:

TC#NameOrganismal TypeExample
2.A.5.1.1

High affinity zinc-regulated zinc uptake transporter, Zrt1 of 376 aas and 8 TMSs.  May be a transceptor with both transport and receptor (signal transduction) functions (Diallinas 2017; Schothorst et al. 2017). Activated at the transcriptional level by Yap1 and Ace1 (Gomes et al. 2005). Zrt1 may also transport, or influence the uptake of Cd2+ (Gomes et al. 2005).

Yeast, animals, plants

Zrt1 of Saccharomyces cerevisiae

 
2.A.5.1.10

ZIP family porter of 392 aas

Stramenopiles

ZIP family member of Phytophthora infestans (strain T30-4) (Potato late blight fungus)

 
2.A.5.1.11

Ferrous iron (Fe2+) transporting ZIP family member, LIT1, required for intracellular growth and virulence (Huynh et al. 2006). Also transports other metal ions less efficiently.  Residues involved in targetting and activity have been identified including His108, 283 and 309 (Jacques et al. 2010).

Euglenozoa

LIT1 of Leishmania major

 
2.A.5.1.12

Root iron transporter IRT1 of 364 aas and 9 TMSs.  Has an uncleaved signal peptide that targets the protein to the endoplasmic reticulum for transport to the plasma membrane (Zhang et al. 2014).

Plants

IRT1 of Malus xiaojinensis (apple)

 
2.A.5.1.13

Ferrous iron (Fe2+) uptake transporter of 347 aas and 9 TMSs.  Transports iron and possibly Cd2+ in this hyperaccumulating plant. Induced by iron deficiency and cadmium excess (Plaza et al. 2007).

IRT1 of Noccaea caerulescens (Alpine penny-cress) (Thlaspi caerulescens)

 
2.A.5.1.14

Low affinity zinc-regulated zinc uptake transporter, Zrt2 of 422 aas and 7 TMSs. Active in zinc-replete cells and is time-, temperature- and concentration-dependent.  It prefers zinc over other metals as its substrate (Zhao and Eide 1996).

Zrt2 of Saccharomyces cerevisiae

 
2.A.5.1.15

Zinc transporter, Zrt1 of 468 aas and 7 TMSs.  Receives Zn2+ from the secreted, extracellular zincophore protein, Pra1 for uptake of the metal.  The binding site in Pra1 is in the C-terminal region of this 299 aa protein (Łoboda and Rowińska-Żyrek 2017). Pra1 is a cell surface protein with a single N-terminal TMS involved in the host-parasite interaction during candidal infection. With MP65,  it represents a major component of the biofilm matrix. It sequesters zinc from host tissues and mediates leukocyte adhesion and migration (Citiulo et al. 2012).

Zrt1/Pra1 of Candida albicans and Candida dubliniensis (Yeast)

 
2.A.5.1.16

Zinc uptake transporter of 352 aas and 8 TMSs.  RaZIP1 is a high-affinity plasma membrane transporter specialized in Zn2+ uptake, but also taking up Cd2+ with lower affinity (Leonhardt et al. 2018).

Zip1 of Russula atropurpurea

 
2.A.5.1.17

Zinc/Iron/Cadmium ion transporter protein IRT1 of 355 aas and 9 TMSs.  Regulated by MAP kinase 4 which therefore regulates cell death in the presence of Cd2+ (Zhang et al. 2019).

IRT1 of Nicotiana tabacum (Common tobacco)

 
2.A.5.1.18

ZIP1 of 358 aas and 9 TMSs in a 4 + 5 TMS arrangement.  It transports Zn2+ and is induced by the absence of this ion in the medium (López-Millán et al. 2004).

ZIP1 of Medicogo truncatula

 
2.A.5.1.19

ZIP5 of 374 aas and 9 TMSs in a 4 + 5  arrangement.  It transports both Zn2+ and Fe2+ and is up regulated in medium deficient for Zn2+ and Mn2+.

ZIP5 of Medicago truncatula

 
2.A.5.1.2

Iron regulated Fit1-mediated plasma membrane high affinity Fe2+ uptake transporter, Irt1, of 347 aas and 9 TMSs (also takes up Co2+, Mn2+, Zn2+ and possibly Cd2+) (Korshunova et al., 1999; Schaaf et al., 2006; Halimaa et al. 2014).  It is targetted to the plasma membrane by Sorting nexin1 (Snx1; Q9FG38) (Ivanov et al. 2014). Root-to-shoot iron partitioning in Arabidopsis requires the IRON-REGULATED TRANSPORTER1 (IRT1) protein but not its iron(II) transport function (Quintana et al. 2022).

Plants, animals, yeast

Irt1 of Arabidopsis thaliana

 
2.A.5.1.20

ZIP4 of 372 aas and 9 TMSs in a 4 + 5 TMS arrangement.  Zip4 transports Mn2+ and is induced by the absence of Zn2+ in the external medium (López-Millán et al. 2004).

ZIP4 of Medicago truncatula

 
2.A.5.1.21

Zinc-regulated zinc transporting Zrt2 of 370 aas and 8 TMSs in a 3 + 5 TMS arrangement. It contains an extra-membrane disordered loop, corresponding to the amino acid sequence 126-215. Three Zrt2+ regions in this loop bind Zn2+ and Cu2+ with comparable affinities below pH 5, and therefore, may equally contribute to metal acquisition under the most acidic conditions in which the Zrt2 transporter is expressed (Bellotti et al. 2022).

Zrt2 of Candida albicans

 
2.A.5.1.22

Zinc (ZrfC) transporter of 522 aas and 9 TMSs in a 1 (N-terminal) + 3 (central; residues 200 - 300) + 5 TMSs (C-terminal).  Aspergillus fumigatus, one of the most widespread opportunistic human fungal pathogens, adapts to zinc limitation by secreting a 310 amino acid Aspf2 zincophore, able to specifically bind Zn2+ and deliver it to ZrfC. Garstka et al. 2022 focused on the thermodynamics of Zn2+ complexes with unstructured regions of Aspf2; basing on a variety of spectrometric and potentiometric data, they show that the C-terminal part has the highest Zn(II)-binding affinity among the potential binding sites, and Ni2+ does not compete with Zn2+ binding to this region. The 14 amino acid Aspf2 C-terminus coordinates Zn2+ via two Cys thiolates and two His imidazoles (Garstka et al. 2022). The Aspf2 zincophore protein is a member of the Asp F2 family (TC# 8.A.190).

ZrfC/Aspf2 of Aspergillus fumigatus

 
2.A.5.1.3Zinc/iron uptake transporter, Zip1 (Grass et al., 2005; Grotz et al., 1998)PlantsZip1 of Arabidopsis thaliana (O81123)
 
2.A.5.1.4

Iron-regulated Fit1-mediated (coregulated with Irt1) vacuolar high-affinity Fe2+ efflux (from the vacuole into the cytoplasm) transporter, Irt2 (also transports Zn2+ (Schaaf et al., 2006). The archetypical IRT proteins from angiosperms likely emerged before the origin of land plants during early streptophyte algae terrestrialization, a process that required the evolution of Fe acquisition in terrestrial subaerial settings (Rodrigues et al. 2023).

Plants

Irt2 of Arabidopsis thaliana (O81850)

 
2.A.5.1.5

Zinc (Zn2+) uptake transporter, ZIP8 (Ueno et al. 2010)

Plants

ZIP8 of Oryza sativa (A3BI11)

 
2.A.5.1.6

The Zn2+/Cd2+ transporter, ZNT1 (Nishida et al., 2011).  The histidine-rich loop between TMSs 3 and 4 binds Cu2+ > Zn2+ > Ni2+ (Potocki et al. 2014). Expression of particular transmembrane transporters (e.g., members of the ZIP (ZNT1) and NRAMP (NRAMP4) families) leads to metal tolerance and accumulation in plants (Fasani et al. 2021).

Plants

ZNT1 of Thlaspi caerulescens (Q9M7J1)

 
2.A.5.1.7

The Zn2+/Cd2+ transporter ZNT2 (Nishida et al., 2011)

Plants

ZNT2 of Thlaspi caerulescens (Q92XE7)

 
2.A.5.1.8

Zinc-regulated transporter 1 (High-affinity zinc transport (uptake) protein Zrt1) (Boch et al. 2008).

Yeast

Zrt1 of Schizosaccharomyces pombe

 
2.A.5.1.9

Protein ZntC

Amoeba

ZntC of Dictyostelium discoideum

 
Examples:

TC#NameOrganismal TypeExample
2.A.5.2.1

Golgi Mn2+ homeostasis protein (probably pumps Mn2+ into cytoplasm), ATX2 (Eide, D.J, 1998)

Yeast

ATX2 of Saccharomyces cerevisiae

 
Examples:

TC#NameOrganismal TypeExample
2.A.5.3.1

Growth arrest-inducible protein, ZIP2 of 309 aas.  Zinc dyshomeostasis leads to augmented production of proinflammatory cytokines, promoting chronic inflammation and increasing the susceptibility to age-related diseases. ZIP2 plays a role in the immune system, especially during zinc deficiency, while a polymorphism in the coding region of ZIP2 (Gln/Arg/Leu) is associated with severe carotid artery disease (Giacconi et al. 2015).

Animals

SLC39A2 of Homo sapiens

 
2.A.5.3.10

Zinc transporter 11, ZnT11, of 349 aas and 9 TMSs (Yu et al. 2020).

ZnT11 of Solanum tuberosum (potato)

 
2.A.5.3.11

Zinc (Zn2+) transporter, ZIP1, of 358 aas and 8 TMSs in a 3 + 5 TMS arrangement.

ZIP1 of Plasmodium falciparum

 
2.A.5.3.12

ZIP domain-containing protein of 325 aas and 8 TMSs in a 3 + 5 TMS arrangement.

Zip, zinc- and iron-transporting protein of Plasmodium falciparum

 
2.A.5.3.13

Zinc transporter 2, ZIP2, of 340 aas and 9 TMSs in a 4 + 5 TMS arrangement. SpZIP2 participates in the uptake and accumulation of Cd2+ into cells and might contribute to Cd2+ hyperaccumulation in S. plumbizincicola (Han et al. 2022).

ZIP2 of Sedum plumbizincicola

 
2.A.5.3.2

Zn2+ uptake transporter, Zip1 (abundantly expressed; involved in zinc homeostasis rather than acquisition of dietary Zn2+) (Gaither and Eide, 2000).  Mouse Zip1, 2 and 3 play important noncompensatory roles under conditions of zinc deficiency (Kambe et al. 2008).

Animals

SLC39A1 of Homo sapiens

 
2.A.5.3.3

Zn2+ uptake transporter, Zip3 (poorly expressed; involved in Zn2+ homeostasis) (Dufner-Beattie et al., 2003). This protein plays an ancillary role in zinc homeostasis in mice (Dufner-Beattie et al. 2005).

Animals

SLC39A3 of Homo sapiens

 
2.A.5.3.4

Zinc transporter 1 (ZRT/IRT-like protein 1) (OsZIP1)

Plants

ZIP1 of Oryza sativa

 
2.A.5.3.5Zinc transporter ZIP1 (DrZIP1) (Solute carrier family 39 member 1) (Zrt- and Irt-like protein 1) (ZIP-1)Animals

Slc39a1 of Danio rerio

 
2.A.5.3.6

Zip1 (ZIP42C.1) Zn2+ uptake transporter of 352 aas; Zn/Fe regulated (Lye et al. 2013; Dechen et al. 2015).

Animals

Zip1 of Drosophila melanogaster (Fruit fly)

 
2.A.5.3.7

ZIP family member of 437 aas

Alveolata

ZIP protein of Cryptosporidium parvum

 
2.A.5.3.8

Zip3 or Zip89B Zinc uptake porter of 495 aas.

Animals

Zip3 of Drosophila melanogaster

 
2.A.5.3.9

Putative zinc transporter of 298 aas and 8 TMSs.

Zn2+ transporter of Entamoeba histolytica

 
Examples:

TC#NameOrganismal TypeExample
2.A.5.4.1

Zip4 dietary Zn2+ uptake transporter of 647 aas and 7 TMSs in a 1 (N-terminus) +3 (middle) +3 (C-terminal) TMS arrangement (Acrodermatitis enteropathica zinc-deficiency disease protein) (Dufner-Beattie et al., 2003).  The large cytoplasmic loop is an intrinsically disordered zinc binding domain (Bafaro et al. 2015). A modeled ZIP4 dimer possibly resembles the twelve TMS monomeric PiPT of the MFS, as a likely structural homologue (Antala et al. 2015). Zip4 zinc transporter mutations linked to acrodermatitis enteropathica disrupt function and cause mistrafficking (Kuliyev et al. 2021). A missense variant of SLC39A4 (Zip4) is found in a litter of turkish van cats with acrodermatitis enteropathica (Kiener et al. 2021). hZIP4 is the primary Zn2+ importer in the intestine, but it is also expressed in a variety of organs such as the pancreas and brain. It and a mutant form have been expressed in yeast (Liu et al. 2022). The transmembrane domains mediate oligomerization of the human ZIP4 transporter in vivo (Liu et al. 2022).  A "divide and conquer" strategy has been applied to ZIP4 to study the extracellular domain (ECD) and the transmembrane domain separately, which has led to the first ECD structure in the entire ZIP family. Duan and Zhang 2023 provided detailed protocols for the expression, purification, and crystallization of ZIP4-ECD from a mammalian species.  Xenotransplanted human organoids identify transepithelial zinc transports, SLC39A4 and A5, as two mediators of intestinal adaptation (Sampah et al. 2024).

Animals

SLC39A4 of Homo sapiens

 
2.A.5.4.10

Zn2+ transporter, Zip5 (540aas; 1+3+3 TMSs; processed to a 3+3 TMS protein) (Basolateral membrane; carries out serosal to mucosal transport).  Xenotransplanted human organoids identify transepithelial zinc transports, SLC39A4 and A5, as two mediators of intestinal adaptation (Sampah et al. 2024).

Animals

SLC39A5 of Homo sapiens

 
2.A.5.4.11

The Zn2+ and Cd2+ uptake porter, ZipB (nonsaturable; electrogenic) (Lin et al. 2010). Water-mediated zinc transport through the ZipB channel sugests an essential role of solvated water molecules in driving zinc coordination dynamics and transmembrane crossing (Gupta et al. 2019). The 3D structure is known for a close ortholog (83% identity) from Bordetella bronchiseptica (Zhang et al. 2023).

Bacteria

ZipB of Bordetella bronchispetica (Q2KXZ6)

 
2.A.5.4.12

ZIP13 Zn influx porter, an 8TMS homodimer with N- and C-termini facing the lumen of the Golgi. Important for connective tissue development. Its loss causes the Spondylocheiro dysplastic form of Ehlers-Danlos syndrome (Bin et al., 2011).

AnimalsSLC39A13 of Homo sapiens
 
2.A.5.4.13

Solute carrier family 39, SLC39 (zinc transporter), member 6, ZIP6.  May be an evoltionary precursor of mammalian prion proteins (Schmitt-Ulms et al. 2009).

Animals

SLC39A6 of Homo sapiens

 
2.A.5.4.14 solute carrier family 39 (zinc transporter), member 12AnimalsSLC39A12 of Homo sapiens
 
2.A.5.4.15

Zinc/iron/manganese/cadmium/selenium transporter ZIP8 (BCG-induced integral membrane protein in monocyte clone 103 protein) (Solute carrier family 39 member 8 (SLC39A8; Zrt- and Irt-like protein 8) (Jenkitkasemwong et al. 2012).  Functions in Cd2+ and Mn2+ uptake, cell toxicity and hypertension (Zhang et al. 2015). Also transports selenium (Liang et al. 2021). Four amino acid residues, V33, G38, S335, and I340 of hZIP8 are mutated in patients with congenital disorders of glycosylation (CDG), caused by low blood Mn2+ levels (Fujishiro et al. 2022). Among the four mutations observed in ZIP8-mutated CDG patients, the S335T and I340N mutations in TMS5 abolished Mn2+- and Cd2+-transport activity, while V33M and G35R mutations did not. Artificial mutations in the metal-binding motif EEXXH in TMS5, which exists in most ZIP transporters, abolished the Mn2+- and Cd2+-transport activity of hZIP8 (Fujishiro et al. 2022). Loss of hepatic manganese transporter ZIP8 disrupts serum transferrin glycosylation and the glutamate-glutamine cycle (Powers et al. 2023). ZIP8 plays a role in systemic iron homeostasis but does not modulate the severity of inflammatory lung injury or the host defense against a common bacterial cause of pneumonia (Zhang et al. 2023). Neuronal SLC39A8 deficiency impairs cerebellar development by altering manganese homeostasis (Choi et al. 2024).

Animals

SLC39A8 of Homo sapiens

 
2.A.5.4.16

Zinc transporter Foi (Protein fear-of-intimacy) (Protein kastchen)

Animals

Foi of Drosophila melanogaster

 
2.A.5.4.17

Zinc importer, ZupT of 291 aas and 6 TMSs (Herzberg et al. 2014).

ZupT of Cupriavidus metallidurans (Ralstonia metallidurans)

 
2.A.5.4.18

Zinc transporter, ZIPT-7.1; regulates sperm activation in nematodes. In spermatids, inactive ZIPT-7.1 localizes to the intracellular membranous organelles, which contain higher levels of zinc than the cytoplasm. When sperm activation is triggered, ZIPT-7.1 activity increases, releasing zinc from internal stores. The resulting increase in cytoplasmic zinc promotes activatioin (Zhao et al. 2018).

 

ZIPT-7.1 of Caenorhabditis elegans

 
2.A.5.4.19

ZIP Zinc transporter of 231 aas and 8 TMSs

ZIP transporter of Lokiarchaeum sp. GC14_75

 
2.A.5.4.2

Zinc transporter, LIV1 (essential for the nuclear localization of the zinc-finger protein Snail, a master regulator of the epithelial-mesenchymal transition in zebrafish gastrulation) (Yamashita et al., 2004)

Animals

LIV1 in Danio rerio (Q6L8F3)

 
2.A.5.4.20

Zinc/Iron transporter, Zip13 (gene: Zip99c) of 355 aas and 8 TMSs. A conserved motif in TMS4 is DNXXH instead of the usual HNXXD; only the former motif, not the latter, allows iron transport (Zhao and Zhou 2019).

Zip13 of Drosophila melanogaster (Fruit fly)

 
2.A.5.4.3

Zip7 Golgi Zn2+ uptake (into the cytoplasm) transporter (Ke4, Slc39a7) (Huang et al., 2005). This protein can substitute for Iar1, the indole acetic acid-alanine resistance protein, of A. thaliana (Lasswell et al., 2000)

Animals

SLC39A7 of Homo sapiens

 
2.A.5.4.4Bidirectional endoplasmic reticular Zn2+ transporter, Yke4 (346 aas; Kumanovics et al., 2006)YeastYke4 (YIL023c) of Saccharomyces cerevisiae (P40544)
 
2.A.5.4.5

Zip14 Zn2+/Fe2+/Mn2+/Cd2+ uptake transporter (mobilized to the sinusoidal membrane of the hepatocyte during acute inflammation) (Jenkitkasemwong et al. 2012; Pinilla-Tenas et al., 2011); KM for Fe2+= 0.002 μM.  The prion gene family may have descended from an ancestral LZT gene (Ehsani et al. 2012).  The gene is upregulated by iron loading (Nam et al. 2013). LIV-1 ZIP ectodomain shedding in prion-infected mice resembles the cellular response to transition metal starvation (Ehsani et al. 2012).  Zip14 promotes cellular assimilation of iron from transferrin (Zhao et al. 2010) and also plays a role in maintaining manganese homeostasis (Xin et al. 2017). SLC39A14 is essential for efficient Mn2+ uptake by the liver and pancreas, and its deficiency results in impaired Mn2+ excretion and accumulation of the metal in other tissues (Jenkitkasemwong et al. 2018). Mutations cause hypermanganesemia associated with infantile onset dystonia (Juneja et al. 2018).  SLC39A14 and SLC30A1 increased cellular sensitivity to cadmium (Ferdigg et al. 2025).

.

Animals

SLC39A14 of Homo sapiens

 
2.A.5.4.6

Zinc transporter, Zip10 (plays an essential role in the migratory activity of highly metastatic breast cancer cells) (Kagara et al., 2007).  May be an evolutionary precursor of prion proteins in mammals (Schmitt-Ulms et al. 2009).

Animals

SLC39A10 of Homo sapiens

 
2.A.5.4.7The indole acetic acid-alanine resistance protein 1, Iar1 (Lasswell et al., 2000)PlantsIar1 of Arabidopsis thaliana (Q9M647)
 
2.A.5.4.8The divalent cation (M2+): bicarbonate (HCO3-) transporter (M2+:HCO3- = 1:2). Transports Cd2+ and Zn2+, and probably Cu2+, Pb2+, and Hg2+ (based on competitive inhibition studies (Liu et al., 2008))AnimalsZip8 of Mus musculus (Q91W10)
 
2.A.5.4.9

Probable Zn2+ transporter, Zip13 (SLC39A13). Mice deficient in Zn transporter Slc39a13/Zip13 show changes in bone, teeth and connective tissue reminiscent of the clinical spectrum of human Ehlers-Danlos syndrome (EDS) (Fukada et al., 2008).

Animals

Zip13 of Mus musculus (Q8BZH0)

 
Examples:

TC#NameOrganismal TypeExample
2.A.5.5.1

Broad specificity heavy metal divalent cation uptake transporter, ZupT (Fe2+, Co2+, Mn2+, Cd2+ and Zn2+ are transported) (Grass et al., 2005). Point mutations change the specificity and kinetics of metal uptake (Taudte and Grass, 2010). Important for virulence in Salmonella (Karlinsey et al., 2010). ZupT has an asymmetric binuclear metal center in the transmembrane domain; one metal-binding site, M1, binds zinc, cadmium, and iron, while the other, M2, binds iron only and with higher affinity than M1. Using site-specific mutagenesis and transport activity measurements in whole cells and proteoliposomes, Roberts et al. 2021 showed that zinc is transported from M1, while iron is transported from M2. The two sites share a common bridging ligand, a conserved glutamate residue. M1 and M2 have ligands from highly conserved motifs in transmembrane domains 4 and 5. Additionally, M2 has a ligand from transmembrane domain 6, a glutamate residue, which is conserved in the gufA subfamily of ZIP transporters, including ZupT and the human ZIP11. Unlike cadmium, iron transport from M2 does not inhibit the zinc transport activity but slightly stimulates it. This stimulated activity is mediated through the bridging carboxylate ligand. The binuclear zinc-iron binding center in ZupT has likely evolved to enable the transport of essential metals from two different sites without competition; a similar mechanism of metal transport is likely to be found in the gufA subfamily of ZIP transporter proteins (Roberts et al. 2021).

Bacteria

ZupT of E. coli (P0A8H3)

 
2.A.5.5.10

ZIP family Zinc/Iron transporter with 267 aas and 7 or 8 TMSs

ZIP of Desulfovibrio vulgaris

 
2.A.5.5.11

ZupT zinc transporter of 277 aas and 7 or 8 TMSs.

ZupT of Desulfovibrio vulgaris

 
2.A.5.5.12

Fe2+/Zn2+ transporter, ZupT, of 226 aas and 8 - 10 TMSs (Chanket et al. 2024).

ZupT of Clostridioides difficile (strain 630) (Peptoclostridium difficile)

 
2.A.5.5.2

Zinc transporter ZIP11 (Solute carrier family 39 member 11) (Zrt- and Irt-like protein 11) (ZIP-11). In mice, Zip11 mRNA is abundantly expressed in testes and the digestive system including stomach, ileum and cecum. Analysis of cellular zinc content, metallothionein levels, and cell viability under high or low zinc conditions in cells transfected with a murine Zip11 expression plasmid, suggest that Zip11 is a zinc importer (Yu et al. 2013). ZIP11 may have a zinc and iron binuclear transport center for iorn and zinc (Roberts et al. 2021).

Animals

SLC39A11 of Homo sapiens

 
2.A.5.5.3

Zinc-regulated transporter 3, Zrt3 (Vacuolar membrane zinc transporter)

Fungi

Zrt3 of Saccharomyces cerevisiae

 
2.A.5.5.4Probable zinc transporter zip2Yeastzip2 of Schizosaccharomyces pombe
 
2.A.5.5.5Zinc transporter ZupT

Verrucomicrobia

ZupT of Akkermansia muciniphila

 
2.A.5.5.6

ZIP11, Zinc permease of 251 aas and 8 TMSs (Hudek et al. 2013).  Transports zinc as well as cadmium, cobalt, copper, manganese and nickel.

Cyanobacteria

Zinc/Iron permease of Nostoc punctiforme

 
2.A.5.5.7

Zip family protein of 651 aas, ZIL2

Green Algae

ZIL2 of Chlamydomonas reinhardtii (Chlamydomonas smithii)

 
2.A.5.5.8

Zip family homologue of 553 aas and 16 TMSs

Green Algae

ZIP family homologue of Volvox carteri

 
Examples:

TC#NameOrganismal TypeExample
2.A.5.6.1

Zip family member, ZIP9 (SLC39A9) (307aas; 8 TMSs).  The orthologue, Zip9, in the atlantic croaker (Micropogonias undulatus) is an androgen receptor that mediates testosterone-induced apoptosis of female ovarian follicle cells (Berg et al. 2014).  SLC39A9 and PIK3C3 as crucial entry factors for Ebola virus infection (Gong et al. 2024).

Animals

SLC39A9 of Homo sapiens

 
Examples:

TC#NameOrganismal TypeExample
Examples:

TC#NameOrganismal TypeExample