Genome Wide Identification, Phylogeny and Expression of Zinc Transporter Genes in Common Carp

Overview

Journal PLoS One

Specialties General Medicine
Science

Date 2015 Jan 1

PMID 25551462

Citations 3

Authors

Yanliang Jiang

Songhao Zhang

Shuaisheng Feng

Jinsheng Sun

Peng Xu

Affiliations

Soon will be listed here.

Abstract

Background: Zinc is an essential trace element in organisms, which serves as a cofactor for hundreds of enzymes that are involved in many pivotal biological processes including growth, development, reproduction and immunity. Therefore, the homeostasis of zinc in the cell is fundamental. The zinc transporter gene family is a large gene family that encodes proteins which regulate the movement of zinc across cellular and intracellular membranes. However, studies on teleost zinc transporters are mainly limited to model species.

Methodology/principal Findings: We identified a set of 37 zinc transporters in common carp genome, including 17 from SLC30 family (ZnT), and 20 from SLC39 family (ZIP). Phylogenetic and syntenic analysis revealed that most of the zinc transporters are highly conserved, though recent gene duplication and gene losses do exist. Through examining the copy number of zinc transporter genes across several vertebrate genomes, thirteen zinc transporters in common carp are found to have undergone the gene duplications, including SLC30A1, SLC30A2, SLC30A5, SLC30A7, SLC30A9, SLC30A10, SLC39A1, SLC39A3, SLC39A4, SLC39A5, SLC39A6, SLC39A7 and SLC39A9. The expression patterns of all zinc transporters were established in various tissues, including blood, brain, gill, heart, intestine, liver, muscle, skin, spleen and kidney, and showed that most of the zinc transporters were ubiquitously expressed, indicating the critical role of zinc transporters in common carp.

Conclusions: To some extent, examination of gene families with detailed phylogenetic or orthology analysis could verify the authenticity and accuracy of assembly and annotation of the recently published common carp whole genome sequences. The gene families are also considered as a unique source for evolutionary studies. Moreover, the whole set of common carp zinc transporters provides an important genomic resource for future biochemical, toxicological and physiological studies of zinc in teleost.

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References

Inoue K, Matsuda K, Itoh M, Kawaguchi H, Tomoike H, Aoyagi T . Osteopenia and male-specific sudden cardiac death in mice lacking a zinc transporter gene, Znt5. Hum Mol Genet. 2002; 11(15):1775-84. DOI: 10.1093/hmg/11.15.1775. View

Feeney G, Zheng D, Kille P, Hogstrand C . The phylogeny of teleost ZIP and ZnT zinc transporters and their tissue specific expression and response to zinc in zebrafish. Biochim Biophys Acta. 2006; 1732(1-3):88-95. DOI: 10.1016/j.bbaexp.2005.12.002. View

Zhao L, Zhang Y, Ji P, Zhang X, Zhao Z, Hou G . A dense genetic linkage map for common carp and its integration with a BAC-based physical map. PLoS One. 2013; 8(5):e63928. PMC: 3660343. DOI: 10.1371/journal.pone.0063928. View

Liuzzi J, Lichten L, Rivera S, Blanchard R, Aydemir T, Knutson M . Interleukin-6 regulates the zinc transporter Zip14 in liver and contributes to the hypozincemia of the acute-phase response. Proc Natl Acad Sci U S A. 2005; 102(19):6843-8. PMC: 1100791. DOI: 10.1073/pnas.0502257102. View

Dufner-Beattie J, Kuo Y, Gitschier J, Andrews G . The adaptive response to dietary zinc in mice involves the differential cellular localization and zinc regulation of the zinc transporters ZIP4 and ZIP5. J Biol Chem. 2004; 279(47):49082-90. DOI: 10.1074/jbc.M409962200. View

Petkovic V, Miletta M, Eble A, Fluck C, Mullis P . Alteration of ZnT5-mediated zinc import into the early secretory pathway affects the secretion of growth hormone from rat pituitary cells. Horm Res Paediatr. 2014; 82(4):245-51. DOI: 10.1159/000365924. View

Piletz J, GANSCHOW R . Lethal milk mutation results in dietary zinc deficiency in nursing mice. Am J Clin Nutr. 1978; 31(4):560-2. DOI: 10.1093/ajcn/31.4.560. View

David L, Blum S, Feldman M, Lavi U, Hillel J . Recent duplication of the common carp (Cyprinus carpio L.) genome as revealed by analyses of microsatellite loci. Mol Biol Evol. 2003; 20(9):1425-34. DOI: 10.1093/molbev/msg173. View

Haney C, Grass G, Franke S, Rensing C . New developments in the understanding of the cation diffusion facilitator family. J Ind Microbiol Biotechnol. 2005; 32(6):215-26. DOI: 10.1007/s10295-005-0224-3. View

10.

Holland P, Garcia-Fernandez J, Williams N, Sidow A . Gene duplications and the origins of vertebrate development. Dev Suppl. 1994; :125-33. View

11.

Postlethwait J, Yan Y, Gates M, Horne S, Amores A, Brownlie A . Vertebrate genome evolution and the zebrafish gene map. Nat Genet. 1998; 18(4):345-9. DOI: 10.1038/ng0498-345. View

12.

Aydemir T, Liuzzi J, McClellan S, Cousins R . Zinc transporter ZIP8 (SLC39A8) and zinc influence IFN-gamma expression in activated human T cells. J Leukoc Biol. 2009; 86(2):337-48. PMC: 2726764. DOI: 10.1189/jlb.1208759. View

13.

Xu P, Wang J, Wang J, Cui R, Li Y, Zhao Z . Generation of the first BAC-based physical map of the common carp genome. BMC Genomics. 2011; 12:537. PMC: 3221725. DOI: 10.1186/1471-2164-12-537. View

14.

Yan G, Zhang Y, Yu J, Yu Y, Zhang F, Zhang Z . Slc39a7/zip7 plays a critical role in development and zinc homeostasis in zebrafish. PLoS One. 2012; 7(8):e42939. PMC: 3418240. DOI: 10.1371/journal.pone.0042939. View

15.

Seve M, Chimienti F, Devergnas S, Favier A . In silico identification and expression of SLC30 family genes: an expressed sequence tag data mining strategy for the characterization of zinc transporters' tissue expression. BMC Genomics. 2004; 5(1):32. PMC: 428573. DOI: 10.1186/1471-2164-5-32. View

16.

Glasauer S, Neuhauss S . Whole-genome duplication in teleost fishes and its evolutionary consequences. Mol Genet Genomics. 2014; 289(6):1045-60. DOI: 10.1007/s00438-014-0889-2. View

17.

Lopez V, Kelleher S . Zinc transporter-2 (ZnT2) variants are localized to distinct subcellular compartments and functionally transport zinc. Biochem J. 2009; 422(1):43-52. PMC: 3381892. DOI: 10.1042/BJ20081189. View

18.

Xu P, Zhang X, Wang X, Li J, Liu G, Kuang Y . Genome sequence and genetic diversity of the common carp, Cyprinus carpio. Nat Genet. 2014; 46(11):1212-9. DOI: 10.1038/ng.3098. View

19.

Gaither L, Eide D . The human ZIP1 transporter mediates zinc uptake in human K562 erythroleukemia cells. J Biol Chem. 2001; 276(25):22258-64. DOI: 10.1074/jbc.M101772200. View

20.

Huang L, Kirschke C, Gitschier J . Functional characterization of a novel mammalian zinc transporter, ZnT6. J Biol Chem. 2002; 277(29):26389-95. DOI: 10.1074/jbc.M200462200. View